Memory, Attention, Emotion, and Executive Functioning PDF

Chapter 9 MEMORY, AT TENTION, EMOTION, AND EXECUTIVE FUNCTIONING It is abundantly obvious here that for longer than we can tell, the truth is immeasurably greater than all the tiny fragments we have so far been able to discover. —Attributed to Pavlov by...

Chapter 9 MEMORY, AT TENTION, EMOTION, AND EXECUTIVE FUNCTIONING It is abundantly obvious here that for longer than we can tell, the truth is immeasurably greater than all the tiny fragments we have so far been able to discover. —Attributed to Pavlov by Luria (1947) Everything should be made as simple as possible, but not simpler. —Attributed to Albert Einstein Memory Systems Attention Executive Functioning Relation of Memory, Attention, and Executive Function Neuropsychology of Emotional Processing Neuropsychology in Action 9.1 Amnesia: The Case of N.A. 9.2 Executive Function Tasks 9.3 The Case of Phineas Gage  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 225 Keep in Mind What integrative and management functions do higher systems serve? If short-term memory is impaired, can information be learned and consolidated into storage? What are the similarities and differences of the models of attention? Is there a cognitive function that could be considered the highest function? What effects on behavior do disorders of “management” and “executive” functions have? Overview This chapter is devoted to higher functional systems that are not specific for sensory modalities. Language and visual perception (see discussion in Chapter 8) are also considered higher functional systems because their full expression depends on additional functional systems such as memory, attention, and executive functioning. However, language and visual perception emerge from sensory-perceptual systems; thus, it is easier to follow their progression when they are discussed with these systems. The sensory and motor systems represent the building blocks on which other systems are constructed and the raw material from which other systems draw; they are the most straightforward and best mapped systems. The systems we discuss in this chapter are integrated with the sensory-perceptual and motor systems but do not depend on any one modality. We refer to the systems here as higher order systems because, evolutionarily, the expres- sion in humans is complex and highly integrated. Most of these systems can be thought of as background management systems. Their functions are important for learning, organizing, setting priorities, planning, self-reflection, and self-regulation. The systems discussed in this chapter include the classic systems or modules of cognitive neuropsy- chology, namely memory, attention, and executive functioning. In addition, we consider the brain and mind expressions of emotional processing. For each system, we discuss the conceptual organization of the sys- tem, as well as known structure–function relations. Memory Systems chological perspective: What do you lose if you lose your memory? One patient we evaluated, a man in his 70s with Memory forms the basis of experience and percep- Alzheimer’s disease, could not remember that his wife had tions of self. It is dynamic and malleable. It allows people died 2 years earlier. All his memories were still of her to travel back in time. How you see yourself, to a large being there. Every time someone mentioned that his wife degree, is a product of the experiences of your life, the was dead, he relived the grieving experience. It is scary to lessons you have learned, and what you remember as imagine waking up and not knowing who you are, who being important. Even what you tell yourself to remem- your friends are, and what has happened in your life. ber to do in the future must incorporate memory. Mem- Consider also what it might be like if you could not en- ory pervades most aspects of human experience. Stories of code new information, if you could not remember what your personal and cultural past are stored in memory; someone said 10 minutes ago, or if you could not register thus, it is a necessary foundation of social communica- the information you needed to take a test or learn a new tion. This section examines the various components of skill. memory and what can happen when aspects of the mem- Memory is an umbrella concept, and it is impossible ory system malfunction. to say categorically that someone has an overall good or When memory is working fluidly, there is little need bad memory. It is simply not a single system. Memory is to notice it. But consider the question from a neuropsy- parceled into subsystems based on ideas of storage and 226 PART TWO | The Functioning Brain processing. Neuropsychologists ask how the brain stores in- instances of retrograde amnesia with relatively spared an- formation over the long term and how it encodes, orga- terograde learning and memory (Levine et al., 1998). nizes, and then retrieves information from memory. In Amnesia can be caused by a number of different prob- many disorders neuropsychologists treat on a daily basis, lems and can take several forms. An example of a circum- memory processing is at issue because memory is a “fragile” scribed lesion causing amnesia is the classic case of N.A. system, affected by many disorders, including most of the (Neuropsychology in Action 9.1). dementias, such as Alzheimer’s disease, toxic conditions, loss of oxygen, and head injury. Scientific understanding of normal memory process- A FRAMEWORK FOR CONCEPTUALIZING ing in the brain has profited greatly from the study of peo- MEMORY SYSTEMS ple afflicted with various memory disorders, especially types of amnesia. However, the term amnesia can refer to Psychology textbooks typically describe memory as hav- more than one type of condition. The “soap opera” ver- ing three main divisions: sensory memory, short-term sion of amnesia occurs when one of the characters gets hit memory (STM), and long-term memory (LTM). Sen- on the head and promptly forgets who she or he is and all sory memory is fleeting, lasting only milliseconds, but its the specific episodes of her or his life. This character in- capacity is essentially unlimited in what may be taken in. variably wanders off to make a new life, including the STM is of limited capacity (7 ⫾ 2 bits of information) development of a new identity. Perhaps, after a time, a and degrades quickly over a matter of seconds if informa- startling event occurs (possibly another blow to the head) tion is not held via a means such as rehearsal, or trans- and the character’s prior memory and identity floods ferred to LTM. LTM, theoretically, is of unlimited capac- back. This type of memory deficit is reminiscent of a psy- ity and is relatively permanent except for models that chiatric dissociative state caused by severe emotional suggest that loss of information through forgetting is pos- trauma, but it is not what occurs with neurologic injury sible. Neuropsychologists are most concerned with LTM or disease. and its disorders because these are the problems most evi- Because neurologic patients acquire their memory denced by patients. Often, STM, as measured by neu- problems in conjunction with a brain injury or disease, it ropsychological tasks, is intact even when there are deficits is important to have terminology that marks the nature of in LTM, although isolated disorders of STM exist. Neu- the patient’s memory before the event and the effect on ropsychological conceptualizations of memory generally memory after the event. Anterograde amnesia is the loss do not consider sensory memory; rather, it is thought of of the ability to encode and learn new information after a as a component of sensory processing. defined event (such as head injury, lesion, or disease Neuropsychology concerns itself with understanding onset). Retrograde amnesia is the loss of old memories how memory systems work in correspondence with from before an event or illness. For example, one of our known brain functioning. An important question con- patients, L.S., experienced a head injury as a result of a cerns the possible existence of anatomically separate sys- car accident and had moderate anterograde amnesia and tems in the brain for such concepts as STM, LTM, mild retrograde amnesia. She had no memory of the car explicit-implicit memory, and episodic-semantic mem- accident and only vaguely remembered the paramedics. ory. One way in which researchers can support the idea She did remember being in the hospital emergency room. of separate structures is by showing a double dissociation After the accident, she had difficulty learning new infor- between behaviors. Research can demonstrate strong evi- mation (anterograde amnesia). She often forgot her physi- dence for different systems if a lesion in an area of the cian’s name, and when she returned to college, she found brain affects one system (LTM) but not the other (STM). it hard to study and perform well on history tests for Evidence is even stronger if researchers can show that a which she had to recall facts and dates. Her mild retro- different lesion results in the opposite dissociation grade amnesia is evidenced by her memory for driving out (affects STM but not LTM). This section focuses on of the grocery store parking lot, which was about five conceptualizations of LTM and short-term working blocks from the accident. However, she remembered noth- memory. We explore evidence for different memory sub- ing else of the short time preceding the accident. Amnesias systems, a division between STM and LTM, and between of this type are common in closed head injury (this con- possible divisions of LTM such as separate declarative/ex- dition is described further in Chapter 13). In general, plicit versus procedural/implicit systems. As we explore anterograde (or a combination of anterograde-retrograde) each subsystem, we also discuss disorders that affect that amnesia is evident with brain injury. However, there are system.  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 227 Neuropsycholog y in Action 9.1 A m nesia: The Case of N.A. by Mary Spiers In 1960, N.A. was 22 years old and was a of just a few minutes ago. If he is distracted hospital for therapy, even after 4 years he was member of the U.S. Air Force. One day while by a passing thought or a passing car, the unable to form a spatial map. He found his working on a model airplane, he suffered an thread of conversation is lost. He has little way much like an adult returning to a child- accident that would affect him for the rest of recollection of the day’s events. If you meet hood neighborhood after years of absence. As his life. His roommate, apparently in a playful again the next day, he probably will not pieces of the visual scenery popped up before mood, took a miniature fencing foil from the remember you or what transpired in your him, he decided if the landmark looked wall, tapped N.A. from behind, and as he previous meeting with him. familiar and turned accordingly. This haphaz- turned around, thrust it forward. Unfortu- N.A. likes to keep his room exactly the ard approach of seeing things sometimes nately for N.A., the tiny foil penetrated the same at all times and spends much time required him to back up or retrace his steps cribriform plate at the top of his nasal cavity obsessively arranging things. He becomes until something looked familiar. and entered his brain. The foil pierced his upset at his mother if she moves the tele- N.A. recognizes that he has memory third cranial nerve, but more important, it phone or one of his model airplanes. He likes problems and is not confused. He knows who made a small lesion in the left dorsomedial things exactly the same so he has a better he is and where he is, but may not know the nucleus of the thalamus. It was quickly chance of finding them. Only after a long day or year. As would be suspected, he has discovered that N.A. was amnesic (retro- period and much repetition does he remem- little social life. In a sense, he remains stuck grade) for the past 2 years. In addition, this ber something. If N.A. saw you every day, after in time. Most of his memories are from the minute injury left him with a devastating a period of time he might recognize you, but 1950s. When he fantasizes, he thinks of impairment in his ability to register new still might not know your name. He has only a Betty Grable. He does not know of the people verbal memories (anterograde amnesia). sketchy memory of events that have tran- or events since then. However, N.A. remains In meeting him, the casual observer may spired since 1960. For example, he has a optimistic about his situation and rarely uses not initially suspect there is anything wrong. vague idea that Watergate was a political notes because he wants to work on his N.A.’s intelligence quotient (IQ) is in the high scandal in “Washington or Florida” but recalls memory. average range and he exhibits good social no other details. Because N.A.’s injury is in the This case demonstrates that even a very skills. Furthermore, he is friendly, polite, and left dorsomedial nucleus, he shows more small lesion, strategically placed, can cause has a good sense of humor. But after talking verbal than visual memory deficits. Interest- a devastating problem of memory. Kaushall, with him for a few minutes, it becomes ingly, when he had to learn a new route from Zetin, and Squire (1981) have reported the apparent that he does not remember details his house to the Veterans Administration complete case of N.A. Various theoretical conceptualizations parcel LTM into LONG-TERM MEMORY subsystems (Figure 9.1). Squire (Squire & Cohen, 1984; A problem that is inherently confusing in studying mem- Squire & Butters, 1992) and other investigators advocate ory is the multiple terms scientists use to describe the pos- for a structural–functional difference between declarative sible subcomponents of LTM. Cognitive psychologists, and nondeclarative memory. neuropsychologists, neurologists, and the lay public use Declarative memory is explicit and accessible to con- various, and sometimes conflicting, terms. For example, scious awareness. Nondeclarative memory is usually im- when referring to LTM, the lay public often thinks of the plicit, and a person demonstrates it via performance. ability to remember information from the distant past. Squire and Butters (1992) maintain that the domain of However, neuropsychologists are referring to the specific nondeclarative or procedural memory is that of rules and ability to register information (encode), organize the in- procedures, rather than information that can be verbal- formation in a meaningful way (storage), and recall or rec- ized, although nondeclarative memory has not been ognize the information when needed (retrieval). Accord- clearly operationally defined and often includes a hodge- ing to this definition, LTM is the ability to learn and podge of tasks such as motor skills learning, mirror read- retain new information. Remote memory, by contrast, ing, and verbal priming. Schacter (1987) differentiates concerns memory for long-past events. between explicit and implicit memories. Recall or 228 PART TWO | The Functioning Brain Memory Declarative memory Nondeclarative/Procedural system memory system (factual information, explicit (actions, perceptual-motor skills, memories) conditioned reflexes, implicit memories) Example: Riding a bicycle Semantic Episodic memory system memory (dated recollections of system personal experiences) (general knowledge, Example: First kiss stored undated) Example: Lincoln gave Gettysburg Address Figure 9.1 Long-term memory (LTM) taxonomy. Theories of anatomically separate LTM stores have included the noted distinctions. (From Weiten, W.. Psychol- ogy: Themes and variations [p. 291, Figure 7.28]. Pacific Grove, CA: Brooks/Cole.) recognition, through verbal or nonverbal means, directly nondeclarative memory systems. Some also use the terms indicates explicit memories. Conscious awareness is usu- declarative versus procedural or explicit versus implicit in a ally implied, as is intention to remember. People demon- nearly synonymous manner. There is much debate over strate implicit memory by means in which conscious the existence of separate episodic and semantic systems; awareness is not always necessary, such as implicit prim- in fact, although researchers first described these two sys- ing, skill learning, and conditioning. Yet another possible tems as clearly distinguishable conceptually, they now con- distinction within LTM is between semantic and episodic sider the systems to overlap with other memory concepts. memory. Researchers consider both of these to be forms of explicit or declarative memory. Tulving (1972) intro- Declarative Memory duced the distinction between an episodic memory, One of the first questions that come to mind when peo- which refers to individual episodes, usually autobiograph- ple begin thinking about memory is, “Where is memory ical, that have specific spatial and temporal tags in mem- stored in the brain?” This often implies the search for a ory, and semantic memory, which refers to memory for “center” for memory storage in the brain. It also implies information and facts that have no specific time tag refer- that if this center is removed, then all memory is removed. ence. For example, remembering the details and events of This would be like erasing the entire hard disk of a com- your first date involves episodic memory, whereas remem- puter. (Please note that the brain does not operate like a bering the definition of a word relates to semantic mem- computer; in fact, brains build computers!) If all remote ory. With semantic memory, the context in which the memory were removed from the brain, a person would be memory was encoded is generally not present. Thus, most unable to remember his or her language, facts, episodes, of us do not remember the specific setting and people in- names of people, or any other information previously volved when we learned the name of the first president of encoded. From studies of brain-injured individuals, we the United States. know that this does not happen. People may lose pieces of The most neuroanatomically defensible division be- remote memory, but their brains are not “erased.” There is no tween LTM systems is that of declarative/explicit and one memory storage center. Rather, most neuropsychologists  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 229 think of memory as being ultimately stored in the area The medial temporal structures, which are important for where it was first processed (for example, see Squire, 1987). long-term declarative memory, center around the hip- This would imply, for example, that auditory memories are pocampus and medial temporal lobe. The well-documented stored in primary, secondary, or auditory association areas, case of H.M. (Milner, Corkin, & Teuber, 1968; Scoville, and likewise for other functional systems. 1968) best exemplifies what occurs when these structures The function of the declarative memory system is to are damaged. In 1953, at the age of 27 years, H.M. un- process information in such a way as to tag it or consoli- derwent brain surgery to reduce intractable seizures. The date it for storage in the brain. According to this model, surgery involved bilateral removal of the hippocampus when new declarative learning is occurring, information and portions of the surrounding area, which included the from various cortical areas funnels into the structures hippocampal formation (Figure 9.2). The hippocampal responsible for declarative memory. After it is processed, re- formation, or hippocampal complex, includes the hip- turn neural pathways transmit information back to specific pocampus, the dentate gyrus, and the subiculum. In cross cortical areas. section, the hippocampus has a distinctive “sea horse” shape. Information funnels into the hippocampus via the Declarative Model of Encoding and Retrieval— Tulving and entorhinal cortex. In addition, the perirhinal and parahip- coworkers (1994), based on neuroimaging studies of pocampal cortexes adjacent to the hippocampal forma- healthy individuals, developed a model of memory en- tion are believed to have a role in memory. At the time of coding and retrieval, Hemispheric-Encoding-Retrieval- H.M.’s surgery little was known regarding the effects of Asymmetry (HERA). The model proposes that the pre- such surgery on memory. After the surgery, despite the frontal (dorsolateral) region of the left hemisphere is preservation of above-average intelligence, he was pro- primarily involved in episodic encoding, whereas the foundly amnesic for new learning (anterograde amnesia), prefrontal area of the right hemisphere is prominently both episodic and semantic. He was able to recall old activated for retrieval of episodic information. Subse- memories and facts, but new learning was no longer pos- quently, a comprehensive review of 275 positron emis- sible. STM was preserved in that he could retain new in- sion tomography (PET) and functional magnetic reso- formation for a few minutes. However, this information nance imaging (fMRI) studies by Cabeza and Nyberg could not be consolidated into long-term storage. If he (2000) provided partial support for the model. Analysis met someone and then the person left, he would not have of these neuroimaging studies showed that the left pre- any memory of the meeting a few minutes later. As a re- frontal region activated in verbal episodic encoding sult, if he met the person again, it was as if they had met while retrieval of episodic information was right-later- for the first time. H.M.’s amnesia was even more pro- alized (prefrontal region) for both verbal and nonverbal found than N.A.’s, in that he also had difficulty learning contents. In contradiction with the prediction based on new visuospatial information. the HERA model, encoding of nonverbal information The preservation of old memories with medial tempo- yielded bilateral and right-lateral prefrontal activation. ral damage suggests that memories are not stored in the Other regions activated during episodic retrieval in- hippocampus; rather, this structure appears to be involved cluded temporomedial, parietal, medial parietotempo- in the movement of new information into long-term stor- ral, temporal, occipital, and cerebellar areas, highlight- age. PET and fMRI studies (Cabeza & Nyberg, 2000) ing the multiplicity of regions and circuitry involved in show that the left medial temporal region activates during memory retrieval. Unlike episodic retrieval, the recall of the encoding of verbal material, whereas bilateral activa- semantic information is dependent on the left pre- tion is evident for processing of nonverbal contents. Dam- frontal area for both verbal and nonverbal information age to the hippocampus can significantly disrupt declara- (Cabeza & Nyberg, 2000). Similar to episodic retrieval, tive memory, but the extension of damage to the other brain regions are involved in semantic retrieval entorhinal and parahippocampal regions produces even including temporal, anterior cingulate, and cerebellar more severe and long-lasting amnesia. regions. The specific functions of the regions of the medial temporal lobe are not fully known, but research suggests Declarative Consolidation—Three major interconnected con- that they make differential contributions to memory. For stellations of brain structures play a role in consolidating example, the visual association cortex shows significant information into LTM. The first memory centers around projections to the perirhinal cortex, whereas the parietal the medial temporal lobes, the second around the dien- cortex projects to the parahippocampal cortex. These struc- cephalon, and the third in the basal forebrain. tures appear to play specific roles in visual recognition and 230 PART TWO | The Functioning Brain Mammillary body Cingulate gyrus Fornix Amygdala Temporal lobe Fornix Hippocampal a. complex Coronal section of left temporal lobe Lateral tissue CA3 CA2 CA4 CA1 Dentate gyrus Subiculum Third ventricle Entorhinal cortex c. Neocortex b. Figure 9.2 The hippocampal complex. (a) The hippocampal complex is located on the medial surface of the temporal lobe. (b) A coronal section shows the hippocampus as a deep infolding of the temporal lobe. (c) A close- up shows the structures in relation. The hippocampus consists of four parts (CA1-CA4). The pathway to the hip- pocampus from the cortex leads through the entorhinal cortex. ([b] Adapted from Pinel, P. J., & Edwards, M.. A colorful introduction to the anatomy of the human brain [p. 169, Figure 10.1]. Boston: Allyn & Bacon, by permission; [c] adapted from Burt, A. M.. Textbook of neuroanatomy [p. 488, Figure 20.7]. Philadelphia: W.B. Saunders, by permission.)  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 231 spatial memory, respectively (Squire & Knowlton, 2000). terspersed within the substantia innominata. The substan- The hippocampus appears to have a special role in memory tia innominata is a gray and white matter area that sepa- tasks that require the relating or combining of information rates the globus pallidus from the inferior surface of the from different cortical sources, such as the relation of spe- forebrain. It interconnects with the frontal, parietal, and cific objects or events in time and space. temporal cortexes. An important tract coursing through The structures of the diencephalon involved in mem- the substantial innominata is the ventral amygdalofugal ory center around specific nuclei of the thalamus and the pathway, which connects the amygdala to the dorsal me- mammillary bodies of the hypothalamus (Figure 9.3). dial nucleus of the thalamus. The medial septal nucleus The thalamus consists of several nuclei, with the dorsal lies at the precommissural end of the fornix and projects medial nucleus of the thalamus the most often implicated to the hippocampus through the fornix. It most likely af- in memory disorders. Although the dorsal medial nucleus fects memory when damage disrupts information flow to is involved in memory consolidation, there are sugges- the hippocampus. The nucleus of the diagonal band of tions that it may also assist in the initiation and monitor- Broca is a white matter and cell body area located near ing of conscious retrieval of episodic memories (Wenk, the nucleus basalis. It also projects to the hippocampus 2004). Damage to the dorsal medial nucleus is often im- through the fornix. Researchers think these structures are plicated in Korsakoff ’s syndrome and in some cases of spe- important cholinergic memory structures. cific amnesia, such as N.A.’s case (see Neuropsychology in The major declarative memory system is the Papez cir- Action 9.1). Korsakoff ’s syndrome is a consequence of cuit. Papez originally proposed that this looping pathway chronic alcoholism associated with vitamin deficiency was specific for emotional processing. He noticed that the (thiamine). As a result, degeneration of the thalamic dor- clinical presentation of intense emotional symptoms in somedial nucleus and the mammillary bodies occurs. animals with rabies (derived from Latin meaning “rage”) Patients with Korsakoff ’s syndrome exhibit significant an- was associated with lesions in several limbic system struc- terograde and retrograde amnesia, although certain forms tures, specifically the hippocampus. Today, researchers of nondeclarative memory (for example, procedural mem- know this loop has more to do with consolidating infor- ory) are preserved. Moreover, there are cases of damage mation in memory than as a primary emotional proces- specific to the diencephalon region resulting in amnesia, sor. Information from the cortex and higher cortical asso- such as N.A.’s case (see Neuropsychology in Action 9.1). ciation areas enters the circuit through the cingulate The basal forebrain is the third area implicated in long- gyrus, moves to the parahippocampal gyrus, and then into term declarative memory processing. As described in the hippocampus through the hippocampal formation. Chapter 5, this area is a subcortical part of the telen- The major output system of the hippocampal formation cephalon surrounding the inferior tip of the frontal horn is the fornix. It contains nearly 1 million fibers and is and is strongly interconnected with limbic structures; some comparable in size with the optic tract (Nauta & Feirtag, neuroscientists consider it part of the limbic system (for ex- 1986). The fornix rises out of the hippocampal complex ample, see Crosson, 1992). The basal forebrain represents a and arches anteriorly under the corpus callosum. The major source of cholinergic output to the cortex. Some in- fornix relays information to the mammillary bodies vestigators have suggested that extensive damage of basal (specifically the medial mammillary nucleus) of the hypo- forebrain structures may be needed to affect memory (Zola- thalamus. From there information is projected to the ante- Morgan & Squire, 1993); thus, looking at the contribu- rior nucleus of the thalamus along the mamillo-thalamic tions of an individual nucleus to memory is probably not tract, from where it then goes to the cingulate gyrus to as profitable as regarding the system as a network. Because complete the circuit. Figures 9.2 and 9.5a show the of its location surrounding the inferior tip of the frontal anatomic location of the structures, and Figure 9.5b pre- horn and that the inferior communicating artery perfuses sents a schematic of the loop. this area, stroke easily affects the basal forebrain. This area It is readily apparent by examining amnesia cases such is important to memory not only for the nuclei within but as H.M. and N.A. that a break in the memory consolida- for the fibers that traverse the area. The basal forebrain also tion circuit can disrupt memory in a manner similar to di- contains numerous connections to the mediotemporal area. rect removal of the hippocampus, which neurologists typi- The basal forebrain structures implicated in memory cally consider the most crucial structure in the system. include the nucleus basalis of Meynert, the medial septal nucleus, the nucleus of the diagonal band of Broca, and Nondeclarative Memory the substantia innominata (Figure 9.4). The nucleus The term nondeclarative memory does not refer to a discrete basalis of Meynert includes a group of large neurons in- memory system as much as it acknowledges that some 232 PART TWO | The Functioning Brain Text not available due to copyright restrictions  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 233 Text not available due to copyright restrictions 234 PART TWO | The Functioning Brain Text not available due to copyright restrictions memory functions operate outside the limbic circuitry of terms do not by themselves encompass the entire range of explicit or declarative memory. Researchers have variously nondeclarative memory, researchers prefer the less specific referred to the opposite of limbic circuitry–based memory term (see Squire, 1994). Neurologists also know that a as “habit memory” (Mishkin, Malamut, & Bachevalier, single lesion cannot erase all nondeclarative memory, as it 1984), “procedural memory” (Cohen, 1984), and “im- may for declarative new learning. Although it is premature plicit memory” (Graf & Schacter, 1985). The variety of to present a neuroanatomic classification scheme, scien- memory functions this term encompasses most likely re- tists can describe some aspects of nondeclarative memory flects a collection of different abilities, not necessarily mu- with respect to brain structures, particularly subcortical tually exclusive, and perhaps dependent on different pro- basal ganglia areas. cessing systems. For example, implicit memory implies Researchers observing H.M. noticed that despite se- influence by prior experience without conscious aware- vere amnesia for declarative information, H.M. improved ness of the event. Procedural learning concerns the learn- with practice on certain perceptual motor tasks (Milner ing of procedures, rules, or skills manifested through per- et al., 1968; Scoville, 1968). He was learning, with prac- formance rather than verbalization, although conscious tice, without conscious recognition of this learning. If his awareness may aid procedural learning. Because these amnesia had been total, examiners would have expected  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 235 that each presentation of the task would be performed as as implicit priming. For example, in the word stem com- if it were brand new. One area of nondeclarative memory pletion priming paradigm, a list of words is first presented involves perceptual motor adaptation and skills acquisition. (for example, church, parachute, clarinet, and so on). Be- Many amnesiacs, such as H.M., show a normal learning cause of the severe amnesia, the person’s memory is poor curve as they practice the pursuit rotor and reverse mirror- when examiners demand recall in a declarative task. Ex- reading tasks. The pursuit rotor requires the examinee to aminers then give patients three-letter word stems (for ex- keep a stylus on a spinning disk, much like having to hold ample, chu____, par____, cla_____) and ask them to a place on a record on a turntable. Reverse mirror reading make a word by completing the stems. “Primed” patients requires an individual to trace a maze while looking at it with Korsakoff ’s syndrome were more likely to complete through a mirror. Perceptually, amnesiacs also show nor- the stem with a word they had already seen than were un- mal adaptive behavior when wearing visual prisms. Be- primed examinees, despite the same level of declarative cause prisms distort visual input, simple acts such as amnesia for the words. Perceptual priming also appears in reaching for an object are misdirected at first. The visual the quicker recognition of fragmented objects (such as motor system must quickly learn to “retune” the system those presented in Chapter 8 for testing apperceptive ag- so that it again correctly targets reaching according to the nosics) or of words (see Figure 9.6 for examples of prim- new visual information. Interestingly, amnesiacs can do ing stimuli). Similar to patients with Korsakoff ’s syn- this performance learning and adaptation despite severe drome, amnesic patients with damage to medial and declarative amnesia. However, amnesiacs do not show diencephalic brain areas often show unimpaired implicit normal nondeclarative skill learning for all tasks. For perceptual priming. example, investigations (Gabrieli, Keane, & Corkin, Perceptually based implicit priming is associated with 1987; Xu & Corkin, 2001) of H.M.’s performance on a decreased activity of the posterior neocortex. It has been complex, nondeclarative, problem-solving task (Tower of theorized that the decreased activation of the posterior neo- Hanoi) did not find evidence of consistent improvement cortex reflects a reduction in neural resources needed to across learning trials or mastery of the task. process the content when it recurs, because a visual trace Further support for a nondeclarative memory system remains from the original presentation of the material is provided by the differential performance of patients (Squire & Knowlton, 2000). Notably, implicit priming is with amnesia, Huntington’s disease, and Parkinson’s dis- ease on a measure of serial reaction-time skill learning (Schacter & Curran, 2000). The patients were required to press one of four keys when illumination occurred above a key. The patient groups were not aware that there was a repeating sequence of illumination; yet, across learning trials, the patients with amnesia demon- strated improved performance as evidenced in decreased key press reaction times. In contrast, patients with Huntington’s and Parkinson’s diseases showed impaired learning. Subcortical striatal pathology is central to both Huntington’s and Parkinson’s diseases, suggesting the involvement of this region in serial reaction-time learning. Functional imaging studies have confirmed that serial reaction-time skill learning is supported by the striatal region and circuitry. Other regions that exhibit learning-related changes during serial reaction-time skill learning primarily involve the neocortex (primary motor, supplementary motor, premotor, parietal and occipital cor- tices). These changes suggest that serial reaction-time learning involves changes in perceptual and motor areas Figure 9.6 Amnesiacs who have deficient declarative memory supporting visually guided movements (Schacter & may still have intact implicit memory as they demonstrate by quickly recognizing fragments of previously presented words. Curran, 2000). (Reproduced from McCarthy, R. A., & Warrington, E. K.. Cogni- Researchers also noticed that severely amnesic patients tive neuropsychology [p. 302, Figure 14.3]. San Diego: Academic with Korsakoff ’s syndrome showed a phenomenon known Press, by permission.) 236 PART TWO | The Functioning Brain not synonymous with recognition memory (identification withdraw their hand when the doctor extends his or her of target stimuli when presented with other nontarget stim- hand at a second meeting even though they may not con- uli). Recognition memory appears to involve the encoding sciously recall the association between shaking hands with of phonetic or semantic declarative information, whereas the doctor and being pricked by a pin. priming depends on the visual features of the presented con- Whether the same brain circuitry governs all aspects tent. In addition, different brain systems are believed to sup- of nondeclarative memory is not fully understood. How- port the two types of memory. An example of recognition ever, evidence suggests that structures supporting nonde- memory would be asking a person to memorize a list of clarative memory are probably evolutionarily and onto- words, and then presenting the words, at a later time, ran- logically older and more primitive. We stated earlier that domly interspersed with other nonpresented words. The per- even simple animals without a hippocampal system can son is then asked to identify the words initially learned. learn associative information. Also, preverbal babies Identification of the words originally learned provides a mea- show perceptual-motor learning. Infants between 2 and sure of recognition memory. Case studies show that patients 5 months of age quickly learn that they can kick to move with lesions of the visual extrastriate region demonstrate a mobile attached to one leg (Rovee-Collier, 1993). deficits of visual perceptual priming but intact recognition Many brain structures involved in movement, including memory. Patients with amnesia show the opposite pattern. the cerebellum, the basal ganglia, and the motor strip, Another form of implicit learning is that of “artificial are implicated in motor learning. The cerebellum aids in grammar.” Individuals are presented seemingly random sequential motor learning such as the steps required in strings of consonants without awareness that the organi- learning the piano. The basal ganglion is an important zation of these strings reflects a complex set of rules. The brain circuit responsible for perceptual-motor learning individuals are then informed that the consonant strings and adaptation (Figure 9.7). We discuss this circuit in were generated in accordance with a set of rules. After this explanation, they are exposed to a list of grammatical and Premotor nongrammatical consonant strings and are asked to judge cortex Parietal which strings were formed by the same set of rules. Pa- Basal tients with amnesia perform the task as well as healthy par- ganglia ticipants, even though they have no memory for the conso- Thalamus nant strings used during the training. In addition, patients with basal ganglia disease (for example, Parkinson’s disease) are also able to perform artificial grammar tasks, indicat- ing that striatal pathology is not involved in this form of memory. Research suggests that the posterior neocortex may support the performance of artificial grammar tasks, Frontal Occipital Temporal leading some investigators to pose that this type of learning a. may reflect priming or perceptual processing (Schacter & Curran, 2000; Squire & Knowlton, 2000). The simplest form of nondeclarative memory involves classic or associative learning. This type of memory is evo- Neocortex Premotor cortex lutionarily much older and generally operates on the basis of learned associations. Researchers can demonstrate that even animals whose hippocampus has been removed can Basal ganglia Ventral thalamus learn simple stimulus–response associations. For example, planaria can learn a light–shock pairing and recoil from the light when they subsequently encounter it alone. This Substantia nigra suggests that some basic and primitive aspects of associa- b. tive conditioning are operating. Human amnesiacs pro- duced corroborating evidence for this associative learn- Figure 9.7 (a) The circuitry of nondeclarative perceptual- ing. Amnesiacs who meet a doctor on one occasion do motor learning. (b) Schematic of information flow from the neocortex through the basal ganglia to the premotor cortex. not remember the doctor’s name on the next meeting. (Adapted from Petri, H. L., & Mishkin, M.. Behaviorism, cogni- But, amnesiacs who have been pin-pricked by their doc- tivism and the neuropsychology of memory. American Scientist 82, tor while shaking hands during their first meeting, often 30–37, by permission.)  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 237 Chapter 7 (see the section “Subcortical Motor Process- A moment in time. In the case of amnesiacs such as H.M. ing”). Specifically, this circuit includes the caudate nu- and N.A., this is everything they had. But healthy people cleus, putamen, and globus pallidus. The nuclei of the also travel from moment to moment in a “presence- striatum (caudate and putamen) receive projected infor- chamber” of the mind, using this workspace to assemble mation from cortical sensory areas. From the striatum, information for storage and to connect and reconnect in- information then funnels through the globus pallidus, formation retrieved from LTM, to solve problems or to and then on to the thalamus, where it projects to the pre- make new associations. The difference is that N.A. could motor and prefrontal areas (see Figure 7.11) (Mishkin, no longer connect moments and store aspects of the pres- Malamut, Bachevalier, 1984). Behaviorally, Huntington’s ent as new memory in LTM. The limited capacity and disease best portrays the effect of caudate nucleus dys- short time frame of STM does not accommodate more function of the basal ganglia. Huntington’s disease devel- than a few thoughts, ideas, or bits of information at a ops as a progressive subcortical dementia (see Chapter 15 time. As new bits arrive, they may take the place of others for a thorough description), but caudate nucleus degen- or simply degrade. If there is no linkage between STM eration is the hallmark of Huntington’s disease and is one and LTM, STM floats as an island with only a small area of the first structural changes that computed tomogra- of possible habitation. phy scans identify. The atrophic imaging change appears Researchers interested in memory have debated the at the onset of the choreiform movement disorder. The question of the relation of STM to LTM. Cognitive tasks il- effect of this change appears to target perceptual-motor lustrate that the two appear to measure different areas of learning tasks. In a series of studies spearheaded by Nel- memory. STM is a limited-capacity, rapid-access, input- son Butters (for review, see Squire & Butters, 1992), pa- and-retrieval system analogous to computer RAM (random- tients with Huntington’s disease showed a dissociation in access memory). LTM has unlimited capacity but with a performance from patients with Korsakoff ’s syndrome, restricted rate of input and retrieval much like ROM amnesia, and Alzheimer’s disease. On declarative verbal (read-only memory). The two systems are also coded dif- memory tasks, patients with Huntington’s disease per- ferently. STM uses phonologic coding, relying on an formed relatively better than patients with Korsakoff ’s acoustic code, whereas LTM heavily uses semantic cod- syndrome and Alzheimer’s disease. However, on motor ing, or the associative meaning value of information to be learning tasks, the two cortically impaired groups out- remembered (for review, see Baddeley, 1986). Even performed the patients with Huntington’s disease. This though the two seemingly measure different aspects of double dissociation in functioning prompted the initial memory functioning, a unitary view of memory function- suggestion for separate cortical and subcortical memory ing would argue that LTM depends on STM. That is, structures. Since that time, animal studies and imaging these two systems are viewed as two components of one studies with healthy participants performing motor system linked in a serial fashion; thus, information enter- learning tasks have added evidence for the role of the ing LTM must inevitably flow through STM. In contrast, basal ganglia in implicit memory. a separate system view would argue that LTM and STM are dissociated, so someone could have an LTM deficit with intact STM, whereas another person could have an STM deficit but maintain adequate LTM. Patients with SHORT-TERM MEMORY amnesia with severe LTM deficits often show intact STM. AND WORKING MEMORY On formal testing, they can repeat increasingly longer se- ries of digits and perform well on other tasks presumed to There seems to be a presence-chamber in my mind test STM. However, other patients have a specific STM where full consciousness holds court, and where two or deficit with preserved LTM. This is some of the most con- three ideas are at the same time in audience, and an vincing evidence that STM and LTM are anatomically ante-chamber full of more of less allied ideas, which is separate. situated just beyond the full ken of consciousness. Out of Patients with a pure STM deficit are rare. However, re- this ante-chamber the ideas most nearly allied to those searchers have reported cases with exactly this problem (for in the presence chamber appear to be summoned in a example, see Shallice & Warrington, 1970; Basso, Spinnler, mechanically logical way, and to have their turn of Vallar, & Zanobio, 1982). Shallice and Warrington (1970) audience. reported the case of K.F., a patient who suffered a left pos- —Francis Galton (1883) terior temporal lesion that left him with a greatly reduced STM capacity for verbal information. He had a profound 238 PART TWO | The Functioning Brain STM deficit, having a digit span length of about two, Central rather than the usual seven bits of information. He also Executive demonstrated conduction aphasia whereby he could not repeat sentences. Surprisingly, K.F. showed a normal ver- bal learning curve with practice, indicating intact storage of information in LTM. It is difficult to reconcile K.F.’s Visuo-spatial Episodic Phonological performance with theories posing that verbal STM and sketch-pad Buffer loop LTM use the same anatomic structure, but in different ways. K.F.’s performance also challenges models that seri- ally link STM and LTM and, conversely, provides sup- Visual Episodic Language port for models that postulate that verbal STM and LTM semantics long-term are separate or parallel systems. memory The notion of STM as a component of LTM has grad- ually given way to ideas that now refer to working mem- Figure 9.8 A simplified representation of Baddeley’s working memory model. (Adapted from Baddeley, A.. Fractionating the ory (Baddeley, 1986) as a distinct system encompassing central executive. In D. T. Stuss & R. T. Knight [Eds.], Principles of some of the capacity limitations of STM, but that is a dy- frontal lobe functioning [p. 256, Figure 16.4]. New York: Oxford Univer- namic system also influencing aspects of attention and ex- sity Press, by permission.) ecutive functioning. Several distinctions differentiate STM (sometimes called short-term span) from working mem- ory. First, a cognitive (mental) representation of informa- deficit in Alzheimer’s disease. The attention-controlling tion is held “on line” in temporary store (similar to STM). functions of the central executive system involve focusing, Second, the cognitive representations are subjected to shifting, and dividing attention and interfacing with LTM. some form of mental manipulation or transformation. There are also two modality-specific “slave” systems. The Third, attentional and inhibitory control is necessary for articulatory phonologic loop stores speech-based infor- the protection of the on-line cognitive representations, mation and is important in the acquisition of vocabulary. manipulations, and transformations from external or in- The visuospatial sketch pad manipulates visual and spa- ternal inference. Fourth, the cognitive manipulations or tial images. Recently, Baddeley (2000, 2002) extended the computations often involve using information drawn from model to include a fourth component, the episodic buffer long-term storage. To understand working memory, con- (see Figure 9.8). The episodic buffer is a temporary and sider the following: You are presented a multiplication limited capacity storage system whose posited function is problem to solve mentally such as multiplying 234 by 354. to hold and integrate information of different modalities When performing this problem, you will hold a mental (for example, visual and auditory) through linkage with representation of the problem in short-term storage. As LTM. The central executive controls this buffer and uses you maintain this mental representation while performing conscious awareness as a primary retrieval strategy. For ex- the necessary computations to solve the problem, you will ample, if you are asked to recall a series of numbers pre- need to intensely concentrate and, at the same time, block sented in word form, and you are able to categorize the out any internal or external stimuli that could disrupt your numbers into meaningful groups based on associations in focus. Simultaneously, you will draw from LTM the ap- long-term storage, memory recall will be enhanced. Thus, propriate multiplication facts and the mathematical opera- if numbers are visually presented in word form—fourteen, tions needed to solve the problem. Because of the dynamic ninety-two, nineteen, forty-one—and you draw from and effortful cognitive processes involved in working LTM the numeric representation of historically significant memory, Moscovitch and Winocur (2002) believe that it dates and group the numbers as 1492 (Columbus discov- would be more aptly named “working-with-memory.” ers America) and 1941 (beginning of the World War II), Alan Baddeley’s (2001, 2002) seminal research and the- you have integrated verbal and visual information through orization has substantially enhanced our understanding of linkage with associative information held in LTM. working memory. Working memory is integral to a wide Neuropsychologically, the phonologic loop and the vi- range of cognitive tasks from reading to math to problem suospatial sketch pad link to lateralized modalities in the solving. Baddeley initially conceptualized working mem- brain and to frontal lobe executive processes. The phono- ory as involving three components (Figure 9.8). The cen- logic loop involves auditory-verbal processing and de- tral executive is an attention-controlling system; it super- pends on language-based left hemisphere processes. Like- vises and coordinates slave systems and is the proposed wise, the visuospatial sketch pad is associated with the  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 239 Text not available due to copyright restrictions right hemisphere. The neural substrates that support the line” while it is processed. In these studies, Goldman-Rakic episodic buffer remain to be identified, although frontal tested monkeys’ abilities to recall the position of food in architecture is believed to play a crucial role (Baddeley, one of two food wells after a short delay of several sec- 2002). Goldman-Rakic’s (1988) groundbreaking work in onds. Figure 9.9 shows the general paradigm of the study. primate models of working memory points to the dorsolat- Simultaneous recordings from neurons in the dorsolat- eral prefrontal cortex as the area that holds information “on eral prefrontal area continued to fire during the delay 240 PART TWO | The Functioning Brain until the action of food selection was completed. Since inner thoughts. Nonetheless, if you “pay attention,” you Goldman-Rakic’s work, PET and fMRI studies have sup- can orient to a small sample of the incoming information plied confirmation in humans that the prefrontal cortex and ignore most of the other input. In this way, attention activates during working memory tasks (Jonides et al., operates as a gateway for information processing. Atten- 1993; Smith, Marshuetz, & Geva, 2002). For example, tion allows orienting to, selecting, and maintaining focus based on neuroimaging research, Petrides (1998) has iden- on information to make it available for cortical processing. tified two areas of the prefrontal cortex that are involved The neuropsychology of attention historically has in support of working memory. The first area, the ventro- been a confusing subject because there are so many sub- lateral prefrontal cortex (Brodmann’s areas 45 and 47/12), sets of attentional processing and many possible defini- activates when dynamic (strategic) retrieval of informa- tions of attention. The term attention can refer to a general tion from posterior brain regions is required; that is, when level of alertness or vigilance; a general state of arousal; there is a conscious effort to retrieve specific information orientation versus habituation to stimuli; the ability to in accordance with the individual’s intentions and plans. focus, divide, or sustain mental effort; the ability to target Thus, the ventrolateral cortex is actively involved in the processing within a specific sensory arena (such as visual selection, comparison, and judgment of information held attention or auditory attention); or a measure of capacity. in memory. In contrast, the mid-dorsolateral frontal cor- Researchers have also asked whether attention implies a tex (Brodmann’s areas 46 and 9) activates when informa- general state of cortical tone or energy, or functions as a tion is to be maintained on line for the purpose of moni- network or set of specific structures or networks within toring and manipulation. Jointly, these two areas provide the brain. Attentional processing does not imply a unified the foundation for higher order processes involved in the system, and most researchers now view it as a multifac- planning and organization of behavior. eted concept that implies multiple behavioral states and The move from conceptualizing STM as a storage ca- cortical processes that various subsets of cerebral struc- pacity system to that of working memory as a dynamic, tures control. integrated system entailing both lower and higher order In many types of brain dysfunction, efficiency of the processes highlights the interrelated nature of brain sys- brain to process information diminishes. Sometimes peo- tems. Other memory processes such as prospective mem- ple cannot sustain attention to one particular stimulus for ory (the memory for future intention), temporal memory longer periods or cannot select information (selective at- (memory for information in time order), and source mem- tention) from competing sources. This impairment may ory (memory for context) also rely on frontal lobe and ex- be minimally present and detected only through formal ecutive functioning processes. The next section discusses neuropsychological testing, or may be profound and easily attention, a major higher function that is essential to the noticeable by any observer. efficiency of mental processing. Neuropsychological theories of attentional processing (for example, see Mesulam, 1981; Posner & Petersen, 1990) usually consider the role of the reticular activating system (RAS) in cortical arousal, subcortical and limbic Attention system structures (particularly the cingulate gyrus) in reg- ulation of information to be attended to, the posterior parietal lobe system in focusing conscious attention, and Everyone knows what attention is. It is the taking the frontal lobes in directing attentional resources. They possession of the mind in clear and vivid form of one out also give the right hemisphere prominence as an atten- of what seem several simultaneous objects or trains of tional processor. Theorists have not yet worked out any thought. one-to-one correspondence between levels of attentional —William James (1890) behavior and brain structures or networks. Rather, they can describe general subsets of brain systems related to at- Moving about the world, people confront a flood of infor- tentional functioning. mation that the nervous system cannot treat equally. Your brain must target or “spotlight” specific material to process SUBCORTICAL STRUCTURES and tune out the irrelevant information. For example, when INFLUENCING ATTENTION you stop to talk to a friend in a hallway, you may hear com- peting sounds of others talking and people walking down The RAS regulates the level of cortical activation or the corridor. You may also be preoccupied by your own arousal—a necessary first step in attentional processing.  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 241 With its genesis in the midbrain and its ability to project DiGirolamo (1998) pose that the basal ganglia is involved to large cortical areas, the RAS sets a general cortical tone. in shifting or switching sets, and thus is a component of Researchers can observe and categorize this arousal into the act of orienting to stimuli. brain wave types (beta, alpha, theta, and delta) by their frequency as measured by an electroencephalograph THE CEREBRAL CORTEX AND ATTENTION (EEG). In a general way, sensory input “charges” the RAS. If the brainstem is processing sensory input, the RAS The attentional issues of most interest to human neu- maintains high cortical activation. However, lack of sen- ropsychology generally concern the higher levels of atten- sory input does not necessarily make one drowsy. In fact, tional processing coordinated by the cerebrum, including even with constant sensory input there can be habitua- focused attention, the ability to alternate and divide at- tion. Those who live on a noisy street grow accustomed tentional processes, and the ability to sustain attention. to the sound, but a sudden silence will cause the brain to Focused attention is the ability to respond and pick out orient to the change in sound patterning. Daily bio- the important elements or “figure” of attention from the rhythms of 90 minutes of relatively higher and lower “ground” or background of external and internal stimula- alertness also cycle throughout the day, and circadian tion. Focused attention also implies a measure of concen- rhythms control the sleep/wake cycle through the RAS. tration or effortful processing. A basketball player who We discuss these changing levels of cortical tone further can concentrate on making a free throw, while tuning out in our discussion of sleep (see Chapter 16). If a person is the crowd, is a good example of high focus. However, awake and alert, general level of arousal is more of a back- even the most ordinary event of noticing requires cogni- ground issue than a central one in the neuropsychology tive focus. People are frequently called on to alternate and of attentional processing. However, the RAS also plays a divide attention in the course of daily activities. For ex- role in anticipatory responding. Researchers have hypoth- ample, a receptionist who must switch back and forth be- esized that the RAS may send a preparatory signal to the tween answering the phone and talking with customers cortex to alert it to receive stimuli, and thus put it in a must use alternating attention while mentally holding a heightened state of readiness to receive. Lesions to the place to return to the other activity. Divided attention RAS can result in lowered alertness or coma. Chapter 13 requires partialing out attentional resources at the same discusses coma in greater detail. time rather than switching back and forth, however Neuroscientists are also identifying the role of other quickly. A good example is driving a car, listening to a subcortical structures in attention. Although the precise radio, and talking with a passenger. Researchers have de- functions that these structures play in attentional func- bated whether divided attention is, in fact, possible, or tioning remains to be specified, several interpretations have whether people just manage to shift their attention been posed. Moreover, these regions do not operate in iso- quickly between different stimuli. However, evidence in- lation from one another or from other subcortical and cor- dicates that people can divide attention to some degree. tical structures. For example, support of sustained atten- Sustained attention is the ability to maintain an effortful tion is ascribed to the right fronto-parietal-thalamic neural response over time. It is related to the ability to persist network (Sarter, Givens, & Bruno, 2001). With regard to and sustain a level of vigilance. People who work as air selective visual attention, the thalamus, basal ganglia, and traffic controllers or on assembly-line jobs must have ex- superior and inferior colliculi play a supporting role. The cellent abilities for sustaining attention. thalamus receives activation from the reticular formation Attention can be further characterized by task or in- and projects this arousal to the cortex. Moreover, the thal- formation-processing demands. Tasks that are routinely amus serves to select and relay information from subcorti- processed or overlearned can be performed automatically cal regions to the cortex and, conversely, conveys cortical with minimal conscious thought. Automatic processing neural signals to subcortical regions. Through its gating places minimal demands on attentional resources, and function, it is in position to influence the selectivity of at- since processing demands are low, other tasks can be per- tention (Cohen, 1993). The superior colliculus of the mid- formed concurrently. In contrast, new, unfamiliar, or con- brain plays a role in the reflexive movement of the eyes and flicting tasks require the conscious deployment of mental head when orientating to visual stimuli, whereas the infe- operations. Controlled processing involves the execution rior colliculus is implicated when orientating to auditory of mental operations in a linear or serial manner with a stimuli. Researchers have historically attributed motor significant allocation of attentional resources. Parallel pro- functions to the basal ganglia, but increasingly are recog- cessing of additional tasks is generally not possible (Cohen, nizing their role in cognitive operations. Posner and Aston-Jones, & Gilzenrat, 2004). An experienced driver 242 PART TWO | The Functioning Brain and action, inability to disengage attention, problems in Table 9.1 Disorders That Show Prominent sustained attention or vigilance, distractibility, and an al- Attentional Dysfunction most random tendency to orient to both external and in- ternal stimuli. This set of deficits may cause the loose as- Attention-deficit/hyperactivity disorder sociations in thought processes that schizophrenics Neurologic disease commonly show. Close to half of schizophrenics show no Multiple sclerosis galvanic skin conductance response (SCR), which is ordi- Alzheimer’s disease narily considered an orienting response to novel sensory Parkinson’s disease stimuli (Dawson & Nuechterlein, 1984). Neuropsychol- Head trauma ogists call this subgroup of schizophrenics electrodermal Seizure disorders nonresponders. Nonresponders are more likely to show the Metabolic disorder negative symptoms of schizophrenia including apathy, Hypoglycemic encephalopathy emotional and social withdrawal, and blunted affect. Hyperthyroidism Nonresponders are also more likely to have cortical atro- Psychiatric disorders phy than schizophrenic galvanic skin responders. Interest- Depression ingly, the failure of a psychophysiological skin conduc- Mania tance orienting response to sensory stimulation comes Schizophrenia against a background of chronic elevation of autonomic Right hemisphere stroke: unilateral neglect responses, which implies a generalized hyperarousal in this subgroup. Some investigators suggest (see Cohen, 1993, for review) that the attention deficit in schizophre- does not need to attend to the mechanics of driving while nia may be a primary cognitive dysfunction. conversing with a passenger, because eye, hand, and foot movement associated with driving are well-practiced or MODELS OF ATTENTION “habitual.” A person driving for the first time must com- mit considerable attention to the mechanics of driving A myriad of models have been developed to conceptual- and will find conversing with a passenger to be not only ize attentional functioning. Each model represents a dif- difficult but highly disruptive. ferent theoretical orientation, type of attention, method The disruption of attention is a common complaint of of study, and degree of empirical verification. We present patients who have a variety of disorders. Table 9.1 provides the individual models that Mesulam, Posner, and Mirsky a partial listing of disorders that include attentional dys- developed in order to provide familiarity with neuropsy- function as a prominent component of the symptom pat- chological conceptualizations of attentional functioning. tern. The range of disorders illustrates that attentional dysfunction is easily compromised by neurologic, meta- M e s u l a m’ s M o d e l bolic, and psychiatric disorders. Fatigue, or inability to of Spatial Attention sustain attention to an activity, frequently appears across Mesulam (2000) presents a model of selective, spatial at- a number of more generalized neuropsychological disor- tention that has enhanced our understanding of neu- ders. Patients with neurologic disease, as well as patients ropsychological manifestations of patients exhibiting who have suffered focal or generalized brain insults, often symptoms of attentional neglect. Based on clinical and em- describe mentally wearing out when engaged in tasks that pirical research, Mesulam poses that a neural network in- require persistent effortful attention. People with affective volving the frontal, parietal, and cingulate cortices supports disorders frequently report attention and concentration spatial attention to the extrapersonal world (Figure 9.10). problems. Depressed people often describe drifting off or Each of these regions makes a differential contribution to “spacing out,” so that even when driving they may miss spatial attention. The parietal region generates an internal an exit. Mania is associated with concentration problems spatial representation (sensory map) of the extrapersonal of another sort. Manic people may become so energetic environment, whereas the cingulate cortex assigns and with a relentless “flight of ideas” passing through their regulates motivational and emotional significance to ex- minds that they cannot accomplish anything, because trapersonal elements (Gitelman et al., 1999; Kim et al., they cannot concentrate on one thing at a time. 1999). The frontal cortex, particularly the frontal eye Attentional deficits are also a common concomitant of fields (Brodmann’s area 8) and surrounding areas, modu- schizophrenia. These include perseveration of thought lates and coordinates motor programs for exploration,  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 243 were selectively engaged in orienting attention to inter- nally represented stimuli. Previous research has associated these anterior prefontal regions with working memory operations. Overall, the findings suggest that overlap- ping neural networks are involved in orienting attention to external and internal spatial representations. Lesions in any of the neural components supporting spatial attention can lead to hemispatial neglect, that is, a failure to attend to the contralateral visual field. Hemis- patial neglect generally relates to right rather than left hemisphere injury, suggesting hemispheric asymmetry in the support of spatial attention. The right hemisphere ap- pears specialized for control of spatial attention across the visual field, whereas the left hemisphere’s control is pri- marily limited to the contralateral right side visual field. Posner’s Anterior and Posterior Attention Model Michael Posner presents a model of attention from the per- spective of cognitive psychology and neuroscience. He Figure 9.10 A theoretical schematic of the attentional sys- poses that attention can be defined by three major func- tem. (From Mesulam, M. M.. Principles of behavioral neurol- ogy. Philadelphia: E. A. Davis; reprinted from Cohen, R. A.. The tions: (1) orienting to events, particularly to locations in vi- neuropsychology of attention [p. 334, Figure 14.2]. Reprinted by kind sual space; (2) achieving and maintaining a vigilant or alert permission of Springer Science and Business Media.) state; and (3) orchestrating voluntary actions (Fernandez- Duque & Posner, 2001). Each attentional function is, in turn, supported by separate neural networks, namely, ori- scanning, foveating, fixating, and manipulating (reach- enting, vigilance, and executive networks (Table 9.2). ing) extrapersonal stimuli. Spatial attention requires the Moreover, these attention-neural networks operate inter- integrity of these three cortical areas, as well as their inter- actively with each other and other cortical and subcortical connections with one another and with subcortical regions. regions in the thalamus and striatum. The model thus conceptualizes spatial attention in terms of sensory repre- sentation, motivational importance and expectancy, and motor response. Table 9.2 Posner’s Attention Networks Recently, Mesulam’s model (Nobre, Coull, Maquet, Frith, Vandenberghe, & Mesulam, 2004) was extended to Attention Networks Functions Neural Correlates spatial attention to information held within working memory. Research participants underwent neuroimaging Posterior Orienting to stimuli (fMRI) while performing a spatial working memory task orienting system and a spatial orientation task. The former task required Disengage attention Temporoparietal, superior the orientation of attention to internalized representa- from a stimuli temporal, superior parietal tions of previously encoded stimuli, and the latter re- quired attentional orientation to extrapersonal stimuli. Move to a stimuli Superior colliculus Neuroimaging demonstrated that both tasks recruited Engage new stimuli Thalamus overlapping networks involving the occipital, parietal, and Vigilance attention Achieving and Right frontoparietal frontal cortices. While both spatial tasks activated the su- system maintaining an alert state perior parietal lobe, only the right inferior parietal cortex was selectively activated during extrapersonal attentional Anterior or executive Orchestrating Anterior cingulate, orienting. With regard to the frontal lobes, orienting to attention system voluntary actions lateral and orbitofrontal prefrontal cortex, extrapersonal stimuli activated the premotor and dorsal basal ganglia, thalamus prefrontal cortex, while more anterior prefrontal regions 244 PART TWO | The Functioning Brain When visually orienting to an event in the environ- with lesions in the temporoparietal junction or superior ment, three basic cognitive operations—disengage, move, temporal lobe. This difference was resolved by the discov- and engage—activate. Attention is first disengaged from ery that lesions of the temporoparietal junction or supe- the current event of focus and then moved to the new rior temporal regions impair the ability to disengage from point of focus, where attentional resources are engaged. a stimulus, and then shift attention to a new or novel The operations of disengage, move, and engage are linked stimulus (Posner & Fan, in press). In contrast, lesions of to the parietal, midbrain, and thalamic region, respec- the superior parietal lobe disrupt voluntary shifts of at- tively. Accordingly, the visual orienting system is termed tention following a cue or when searching a visual target. the posterior attention system. This system plays a role There are indications that the orienting system is mod- in conscious attention to portions of your visuospatial ulated, in part, by the cholinergic neurotransmitter ACh field and directs the attention of your eyes to a point in (acetylcholine). ACh is produced by the nucleus basalis of space. The posterior parietal lobe mediates conscious at- the brain forebrain and innervates many cortical areas, in- tention to spatial targets, the midbrain superior colliculus cluding the parietal lobes. Research with primates shows plays a role in moving the eyes from one position to an- that lesions of the nucleus basalis disrupt the disengage- other, and the pulvinar of the thalamus helps select and ment of attention from an ipsilesional cue to engage a tar- filter important sensory information for processing. The get contralateral to the side of the lesion (Fernandez- orienting system is also activated in covert orientation. Duque & Posner, 2001). Covert orientation refers to the spatial engagement of at- Patients with lesions to the right posterior orienting tention to a target without moving the eyes or the head. system frequently fail to attend to the opposite visual For example, if you fixate your eyes on an object, you can field, a condition referred to as hemispatial neglect. As also attend to a peripherally located object without mov- discussed previously, hemispatial neglect is not a sensory ing your eyes or head. deficit to visual input, but rather a failure to attend to half Posner initially ascribed the disengage function to the of the visual field (Figure 9.11). Posner (Posner & Petersen, superior parietal lobe. However, lesion studies showed that 1990) describes this as a problem of engaging, moving, disruption of the disengage function was often associated and disengaging focus to objects in the contralateral field Figure 9.11 A case of hemispatial inattention. (From Honoré Daumier, M.. Babinet prevenu par sa portiere de la visite de la comete. Le Charivari. Courtesy of Museum of Fine Arts, Boston, MA. Reprinted from Cohen, R. A.. The neuropsychology of attention [frontispiece]. New York: Plenum Press, by permission.)  CHAPTER 9 | Memory, Attention, Emotion, and Executive Functioning 245 of vision. In this view, the system does not direct the eyes anterior cingulate and lateral prefrontal cortex in execu- and the brain to engage the left side of space, or to disen- tive attention. One of the trials of the Stroop test presents gage attention from the right side of space. the examinee with the words red, green, and blue printed The vigilance attention system mobilizes and sus- in an incongruous color. For example, the word red is tains alertness for processing high-priority targets and is printed in green type. Reading is an overlearned (auto- important to attentional functioning. For example, if matic) behavior for most adults, and when written text is you were involved in an aerial search for survivors of a presented, decoding occurs quickly and automatically. In boating accident, you would have to maintain a high contrast, naming the color of objects is a less rapid and level of alertness and preparedness to identify a survivor automatic process. When the words red, green, and blue in the expanse of the ocean. In addition, you would need are presented in incongruous color, reading the word is to avoid processing irrelevant information (external or the salient response. If you are asked not to read the internal) to avoid distraction. The neural network sup- words, but to name the incongruous color of the printed porting the vigilance system includes the right frontal words, significant conflict is produced. The anterior cin- and parietal regions of the brain. The neurotransmitter gulate activates, as discussed earlier, to provide the top- norepinephrine, produced by the locus ceruleus of the mid- down inhibitory control and response selection. The lat- brain, is implicated in achieving an alert state and main- eral prefrontal region holds the mental representation of taining attention over time (Fan, McCandliss, Sommer, the “rule” (“Name the color, don’t read the word.”) in Raz, & Posner 2002). working memory to guide the process. The anterior or executive attention system controls Although norepinephrine and ACh are implicated in and coordinates other brain regions in the execution of the support of the alerting and orientating systems, re- voluntary attention. A hierarchy exists for attentional pro- spectively, dopamine is considered the primary neural cessing, with the anterior system passing control to the modulator of the executive or anterior attention system posterior system as needed. The executive attention sys- (Fernandez-Duque & Posner, 2001). Disorders that in- tem orchestrates higher order cognitive functions such as volve disruption of dopaminergic modulation (for exam- task switching, inhibitory control, conflict resolution, ple, schizophrenia) frequently demonstrate dysfunctions error detection, attentional resource allocation, planning, of executive attention. Furthermore, administration of and the processing of novel stimuli. A number of cortical a dopamine agonist to patients with lesions of the and subcortical substrates support the executive attention frontal lobes improves performance on measures of network, although Posner has focused much of his re- executive function (McDowell, Whyte, & D’Esposito, search and theorization on the anterior cingulate and lat- 1998). eral prefrontal cortex (Posner & DiGirolamo, 1998). One of the primary functions of the anterior cingulate relates to the monitoring and resolution of conflict between op- M i r s k y’ s E l e m e n t s erations occurring in different brain areas (Posner & Fan, of Attention Model in press). For example, if an overlearned (automatic) re- Allen Mirsky (National Institute of Mental Health, sponse to a stimulus is to be inhibited in favor of a less Bethesda, MD) developed a neuropsychological model salient response, the anterior cingulate provides the top- that identifies the possible elements of attention and re- down control necessary to initiate the operations of inhi- lates these elements to neuropsychological measures and bition and response selection. Similarly, the anterior cin- the underlying neural systems. Mirsky (1996) proposed gulate activates when a task requires error detection. Thus, that there were three elements of attention: focus-execute, if you were proofreading a recent paper that you had pre- sustain, and shift. A battery of neuropsychological mea- pared for a class, the anterior cingulate would be active sures considered sensitive to attentional functioning was with regard to identifying errors in the text. compiled (Table 9.3) and administered to adult neuropsy- Often, the lateral prefrontal cortex and anterior cingu- chiatric patients and healthy control participants. The test late are jointly activated, depending on the nature of the data revealed four factors, three of which corresponded presented demand or task. The involvement of the lateral with the elements of attention proposed by Mirsky, and prefrontal cortex in the executive attention system relates an additional element that was labeled encode. Subse- to its role in holding mental representations of specific in- quently, the battery was extended to healthy children with formation in temporary memory. This set of cognitive op- measures appropriate to the younger age-group. Once erations is consistent with the definition of working mem- again, four factors were identified, each similar to the ele- ory. The Stroop test (1935) illustrates the roles of the ments of attention identified in the adult studies. 246 PART TWO | The Functioning Brain Table 9.3 Mirsky’s Elements of Attention Subject Group Factor 1: Focus-Execute Factor 2: Shift Factor 3/5: Sustain/Stable Factor 4: Encode Adult WAIS-R Digit Symbol, WCST CPT WAIS-R Digit Span Stroop test, Letter and Arithmetic Cancellation, and TMT-A and -B Child WISC-R Coding and WCST CPT WISC-R Digit Span Digit Cancellation