Biopsychology, Global Edition, 11th Ed - Chapter 8 - PDF

Chapter 8 The Sensorimotor System How You Move Matteo Carta/Alamy Stock Photo Chapter Overview and Learning Objectives Three Principles of LO 8.1 In the context of the sensorimotor system, explain what Sensorimotor Function...

Chapter 8 The Sensorimotor System How You Move Matteo Carta/Alamy Stock Photo Chapter Overview and Learning Objectives Three Principles of LO 8.1 In the context of the sensorimotor system, explain what Sensorimotor Function ­hierarchically organized means. LO 8.2 Explain the important role of sensory input for motor output. LO 8.3 Describe how learning changes the nature and locus of ­sensorimotor control. LO 8.4 Describe and/or draw the general model of sensorimotor function. Sensorimotor Association LO 8.5 Explain the role of the posterior parietal cortex in ­sensorimotor Cortex function and describe what happens when it is damaged or stimulated. LO 8.6 Explain the role of the dorsolateral prefrontal association cortex in sensorimotor function and describe the response properties of neurons in this region of cortex. 212 M08_PINE1933_11_GE_C08.indd 212 22/01/2021 11:09  The Sensorimotor System 213 Secondary Motor Cortex LO 8.7 Explain the general role of areas of secondary motor cortex. LO 8.8 Describe the major features of mirror neurons and explain why they have received so much attention from neuroscientists. Primary Motor Cortex LO 8.9 Describe the conventional view of primary motor cortex ­function and the evidence upon which it was based. LO 8.10 Describe the current view of primary motor cortex function and the evidence upon which it is based. Cerebellum and Basal LO 8.11 Describe the structure and connectivity of the cerebellum Ganglia and explain the current view of cerebellar function. LO 8.12 Describe the anatomy of the basal ganglia and explain the ­current view of their function. Descending Motor LO 8.13 Compare and contrast the two dorsolateral motor pathways Pathways and the two ventromedial motor pathways. Sensorimotor Spinal LO 8.14 Describe the components of a motor unit and distinguish Circuits between the different types of muscles. LO 8.15 Describe the receptor organs of tendons and muscles. LO 8.16 Describe the stretch reflex and explain its mechanism. LO 8.17 Describe the withdrawal reflex and explain its mechanism. LO 8.18 Explain what is meant by reciprocal innervation. LO 8.19 Explain recurrent collateral inhibition. LO 8.20 Describe the phenomenon of walking and the degree to which it is controlled by spinal circuits. Central Sensorimotor LO 8.21 Explain what is meant by a hierarchy of central sensorimotor Programs and Learning programs and explain the importance of this arrangement for sensorimotor functioning. LO 8.22 Describe the various characteristics of central sensorimotor programs. LO 8.23 Explain how the classic Jenkins and colleagues PET study of simple motor learning summarizes the main points of this chapter. LO 8.24 Describe two examples of neuroplasticity—one at the cortical level and one at the subcortical level. The evening before we started to write this chapter, 20 pounds in 2 days. Then, my mind began to wander, and I (JP) was standing in a checkout line at the local market. I started to think about beginning to write this chapter. As I waited, I scanned the headlines on the prominently That is when I began to watch Rhonelle’s movements, and displayed magazines—woman gives birth to cat; flying to wonder about the neural system that controlled them. saucer lands in cleveland shopping mall; how to lose Rhonelle is a cashier—the best in the place. M08_PINE1933_11_GE_C08.indd 213 22/01/2021 11:09  214 Chapter 8 The Case of Rhonelle, the ­Dexterous Cashier Three Principles of I was struck by the complexity of even Rhonelle’s simplest Sensorimotor Function movements. As she deftly transferred a bag of tomatoes to the Before getting into the details of the sensorimotor system, scale, there was a coordinated adjustment in almost every part let’s take a closer look at the three principles of sensorimo- of her body. In addition to her obvious finger, hand, arm, and tor function introduced by Rhonelle. You will better appre- shoulder movements, coordinated movements of her head and ciate these principles if you recognize that they also govern eyes tracked her hand to the tomatoes; and there were adjust- the operation of any large, efficient company—perhaps ments in the muscles of her feet, legs, trunk, and other arm, because that is another system for controlling output that which kept her from lurching forward. The accuracy of these responses suggested that they were guided in part by the pat- has evolved in a competitive environment. You may find terns of visual, somatosensory, and vestibular changes they this metaphor useful in helping you understand the princi- produced. (The term sensorimotor in the title of this chapter ples of sensorimotor system organization—many scientists formally recognizes the critical contribution of sensory input to find that metaphors help them think creatively about their guiding motor output.) subject matter. As my purchases flowed through her left hand, Rhonelle scanned the items with her right hand and bantered with The Sensorimotor System Is Rich, the bagger. I was intrigued by how little of what Rhonelle was doing appeared to be under her conscious Hierarchically Organized control. She made general decisions about which items to LO 8.1 In the context of the sensorimotor system, pick up and where to put them, but she seemed to give no explain what hierarchically organized means. thought to the exact means by which these decisions were carried out. Each of her responses could have been made The operation of both the sensorimotor system and a large, with an infinite number of different combinations of finger, efficient company is directed by commands that cascade wrist, elbow, shoulder, and body adjustments; but some- down through the levels of a hierarchy (see Sadnicka et al., how she unconsciously picked one. The higher parts of her 2017)—from the association cortex or the company presi- sensorimotor system—perhaps her cortex—seemed to issue dent (the highest levels) to the muscles or the workers (the conscious general commands to other parts of the system, lowest levels). Like the orders issued from the office of a which unconsciously produced a specific pattern of muscular company president, the commands that emerge from the responses that carried them out. association cortex specify general goals rather than specific The automaticity of Rhonelle’s performance was a far cry plans of action. Neither the association cortex nor the com- from the slow, effortful responses that had characterized her first days at the market. Somehow, experience had integrated her pany president routinely gets involved in the details. The individual movements into smooth sequences, and it seemed main advantage of this hierarchical organization is that the to have transferred the movements’ control from a mode that higher levels of the hierarchy are left free to perform more involved conscious effort to one that did not. complex functions. I was suddenly jarred from my contemplations by a voice. Both the sensorimotor system and a large, efficient “Sir, excuse me, sir, that will be $78.65,” Rhonelle said, with company are parallel hierarchical systems; that is, they just a hint of delight at catching me mid-daydream. I hastily are hierarchical systems in which signals flow between paid my bill, muttered “thank you,” and scurried out of the levels over multiple paths. This parallel structure enables market. the association cortex or company president to exert con- trol over the lower levels of the hierarchy in more than one way. For example, the association cortex can directly inhibit an eye blink reflex to allow the insertion of a contact As we write this, I am smiling both at my own embar- lens, just as a company president can personally organize rassment and at the thought that Rhonelle has unknow- a delivery to an important customer (see McDougle, Ivry, ingly introduced you to three principles of sensorimotor & Taylor, 2016). control that are the foundations of this chapter: (1) The The sensorimotor and company hierarchies are also sensorimotor system is hierarchically organized. (2) characterized by functional segregation. That is, each level of Motor output is guided by sensory input. (3) Learning the sensorimotor and company hierarchies tends to be com- can change the nature and the locus of sensorimotor posed of different units (neural structures or departments), control. each of which performs a different function. M08_PINE1933_11_GE_C08.indd 214 22/01/2021 11:09  The Sensorimotor System 215 visual monitoring. For example, when carrying a suitcase, he Journal Prompt 8.1 had to watch it to reassure himself that he had not dropped it. Can you think of another effective metaphor for the However, even visual feedback was of little use to him in tasks ­sensorimotor system? requiring a constant force, tasks such as grasping a pen while writing or holding a cup. In these cases, he had no indication of the pressure that he was exerting on the object; all he saw was In summary, the sensorimotor system—like the sensory the pen or cup slipping from his grasp. systems you read about in Chapter 7—is a parallel, func- tionally segregated, hierarchical system. The main difference between the sensory systems and the sensorimotor system is the primary direction of information flow. In sensory sys- Many adjustments in motor output that occur in tems, information mainly flows up through the hierarchy; in response to sensory feedback are controlled unconsciously the sensorimotor system, information mainly flows down. by the lower levels of the sensorimotor hierarchy without the involvement of the higher levels (see Deliagina, Zelenin, & Orlovsky, 2012). In the same way, large companies run Motor Output Is Guided more efficiently if the interns do not check with the com- by Sensory Input pany president each time they encounter a minor problem. LO 8.2 Explain the important role of sensory input for motor output. Learning Changes the Nature and Efficient companies are flexible. They continuously Locus of Sensorimotor Control monitor the effects of their own activities, and they use this LO 8.3 Describe how learning changes the nature and information to fine-tune their activities. The sensorimotor locus of sensorimotor control. system does the same (see Azim, Fink, & Jessell, 2014; Danna & Velay, 2015; Scott, 2016). The eyes, the organs of balance, When a company is just starting up, each individual deci- and the receptors in skin, muscles, and joints all monitor sion is made by the company president after careful con- the body’s responses, and they feed their information sideration. However, as the company develops, many back into sensorimotor circuits. In most instances, this individual actions are coordinated into sequences of pre- sensory feedback plays an important role in directing the scribed procedures routinely carried out by personnel at continuation of the responses that produced it. The only lower levels of the hierarchy. responses that are not normally influenced by sensory Similar changes occur during sensorimotor learning feedback are ballistic movements—brief, all-or-none, high- (see Bassett et al., 2015). During the initial stages of motor speed movements, such as swatting a fly. learning, each individual response is performed under Behavior in the absence of just one kind of sensory conscious control; then, after much practice, individual ­feedback—the feedback carried by the somatosensory responses become organized into continuous integrated nerves of the arms—was studied in G.O., a former darts sequences of action that flow smoothly and are adjusted champion (Rothwell et al., 1982). by sensory feedback without conscious regulation. If you think for a moment about the sensorimotor skills you have acquired (e.g., typing, swimming, knitting, basketball play- The Case of G.O., the Man with ing, dancing, piano playing), you will appreciate that the organization of individual responses into continuous motor Too Little Feedback programs and the transfer of their control to lower levels of An infection had selectively destroyed the somatosensory the CNS characterize most sensorimotor learning. nerves of G.O.’s arms. He had great difficulty performing intri- cate responses such as doing up his buttons or picking up General Model of Sensorimotor coins, even under visual guidance. Other difficulties resulted from his inability to adjust his motor output in light of unantici- System Function pated external disturbances; for example, he could not keep LO 8.4 Describe and/or draw the general model of from spilling a cup of coffee if somebody brushed against him. sensorimotor function. However, G.O.’s greatest problem was his inability to maintain a constant level of muscle contraction. Figure 8.1 is a model that illustrates several principles of The result of his infection was that even simple tasks sensorimotor system organization; it is the framework of requiring a constant motor output to the hand required continual this chapter. Notice its hierarchical structure, the functional M08_PINE1933_11_GE_C08.indd 215 22/01/2021 11:09  216 Chapter 8 Figure 8.1 A general model of the sensorimotor system. Notice its hierarchical structure, functional segregation, parallel descending pathways, and feedback circuits. Association cortex Secondary motor cortex Primary motor cortex Brain stem motor nuclei Muscle Spinal Muscle motor circuits Muscle Descending motor circuits Feedback circuits segregation of the levels (e.g., of secondary motor cortex), Posterior Parietal Association Cortex the parallel connections between levels, and the numerous feedback pathways. LO 8.5 Explain the role of the posterior parietal cortex This chapter focuses on the neural structures that play in sensorimotor function and describe what important roles in the control of voluntary behavior (e.g., happens when it is damaged or stimulated. picking up an apple). It begins at the level of association cor- Before an effective movement can be initiated, certain infor- tex and traces major motor signals as they descend the sen- mation is required. The nervous system must know the orig- sorimotor hierarchy to the skeletal muscles that ultimately inal positions of the parts of the body that are to be moved, perform the movements. and it must know the positions of any external objects with which the body is going to interact. The ­posterior parietal association cortex (the portion of parietal neocortex poste- Sensorimotor Association rior to the primary somatosensory cortex) plays an impor- Cortex tant role in integrating these two kinds of information, in directing behavior by providing spatial information, and Association cortex is at the top of your sensorimotor hier- in directing attention (Freedman & Ibos, 2018; Hutchinson archy. There are two major areas of sensorimotor associa- et al., 2014; Kuang, Morel, & Gail, 2015; Wilber et al., 2014). tion cortex: the posterior parietal association cortex and the You learned in Chapter 7 that the posterior parietal cor- dorsolateral prefrontal association cortex. Posterior parietal tex is classified as association cortex because it receives input cortex and the dorsolateral prefrontal cortex are each com- from more than one sensory system. It receives information posed of several different areas, each with different func- from the three sensory systems that play roles in the local- tions (see Davare et al., 2011; Wilson et al., 2010). However, ization of the body and external objects in space: the visual there is no general consensus on how best to divide either of system, the auditory system, and the somatosensory sys- them for analysis or even how comparable the areas are in tem (see Figure 8.2)—see Sereno and Huang (2014). In turn, humans, monkeys, and rats (see Teixeira et al., 2014; Turella much of the output of the posterior parietal cortex goes & Lingnau, 2014). to areas of motor cortex, which are located in the frontal M08_PINE1933_11_GE_C08.indd 216 22/01/2021 11:09  The Sensorimotor System 217 Apraxia is a disorder of voluntary Figure 8.2 The major cortical input and output pathways of the posterior parietal association cortex. Shown are the lateral surface of the left hemisphere movement that is not attributable to a and the medial surface of the right hemisphere. simple motor deficit (e.g., not to paralysis or weakness) or to any deficit in compre- Areas of secondary Posterior parietal motor cortex association cortex hension or motivation (see Niessen, Fink, & Weiss, 2014). Remarkably, patients with apraxia have difficulty making specific movements when they are requested to Dorsolateral do so, particularly when the movements prefrontal are out of context; however, they can often association cortex readily perform the very same movements under natural conditions when they are not thinking about what they are doing. For example, a carpenter with apraxia who has no difficulty at all hammering a nail during the course of her work might not be able to demonstrate hammering movements when requested to make them, particularly in the absence of a hammer. Although its symp- toms are bilateral, apraxia is often caused by unilateral damage to the left posterior parietal cortex or its connections (Hoeren Frontal et al., 2014; Niessen, Fink, & Weiss, 2014). Visual eye field cortex Contralateral neglect, the other strik- ing consequence of posterior parietal cor- Somatosensory Auditory cortex cortex tex damage, is a disturbance of a patient’s ability to respond to stimuli on the side of the body opposite (contralateral) to the side cortex: to the dorsolateral prefrontal association cortex, to the of a brain lesion in the absence of simple sensory or motor various areas of secondary motor cortex, and to the frontal deficits. Most patients with contralateral neglect often eye field—a small area of prefrontal cortex that controls behave as if the left side of their world does not exist, and both eye movements and shifts in attention (see Moore they often fail to appreciate that they have a problem (see & Zirnsak, 2015; Figure 8.2). Electrophysiological studies Li & Malhotra, 2015). The disturbance is often associated in macaque monkeys and functional magnetic resonance with large lesions of the right posterior parietal cortex, imaging (fMRI) and transcranial magnetic stimulation though damage to other brain regions has also been impli- (TMS) studies in humans indicate that the posterior parietal cated (see Karnath & Otto, 2012). Mrs. S. suffered from cortex contains a mosaic of small areas, each specialized for contralateral neglect after a massive stroke to the posterior guiding particular movements of eyes, head, arms, or hands portions of her right hemisphere (Sacks, 1999). (Man et al., 2015; Wang et al., 2015). Desmurget and colleagues (2009) applied electrical stimulation to the inferior portions of the posterior pari- The Case of Mrs. S., the Woman etal cortexes of conscious neurosurgical patients. At low Who Turned in Circles current levels, the patients experienced an intention to perform a particular action, and, at higher current levels, After her stroke, Mrs. S. could not respond to things on her they felt that they had actually performed it. However, in left—including objects and parts of her own body. For example, neither case did the action actually occur (see Desmurget she often put makeup on the right side of her face but ignored the left. & Sirigu, 2012). Mrs. S.’s left-side contralateral neglect created many Damage to the posterior parietal cortex can produce a problems for her, but a particularly bothersome one was that variety of deficits, including deficits in the perception and she had difficulty getting enough to eat. When a plate of food memory of spatial relationships, in accurate reaching and was put directly in front of her, she could see only the food on grasping, in the control of eye movement, and in atten- the right half of the plate, and she ate only that half, even if she tion (see Andersen et al., 2014; Turella & Lingnau, 2014). was very hungry. However, Mrs. S. developed an effective way ­However, apraxia and contralateral neglect are the two most of getting more food. If she was still hungry after completing a striking consequences of posterior parietal cortex damage. meal, she turned her wheelchair to the right in a full circle until M08_PINE1933_11_GE_C08.indd 217 22/01/2021 11:09  218 Chapter 8 the remaining half of her meal appeared once more directly is the dorsolateral prefrontal association cortex (see Kaller in front of her. Then, she ate that remaining food, or more et al., 2011). It receives projections from the posterior pari- precisely, she ate the right half of it. If she was still hungry after etal cortex, and it sends projections to areas of secondary that, she turned once again in a circle to the right until the motor cortex, to primary motor cortex, and to the frontal eye remaining quarter of her meal appeared, and she ate half of field. These projections are shown in Figure 8.3. that... and so on. Several studies have characterized the activity of mon- key dorsolateral prefrontal neurons while the monkeys identify and respond to objects (e.g., Rao, Rainer, & Miller, Most patients with contralateral neglect have difficulty 1997). The activity of some neurons depends on the char- responding to things to the left. But to the left of what? For most acteristics of objects; the activity of others depends on the patients with contralateral neglect, the deficits in responding locations of objects; and the activity of still others depends occur for stimuli to the left of their own bodies, referred to as on a combination of both. The activity of other dorsolateral egocentric left (see Karnath, 2015). Egocentric left is partially prefrontal neurons is related to the response rather than to defined by gravitational coordinates: When patients tilt their the object. These neurons typically begin to fire before the heads, their field of neglect is not normally tilted with it. response and continue to fire until the response is complete. Some patients also tend not to respond to the left sides Neurons in many cortical motor areas begin to fire in antici- of objects, regardless of where the objects are in their visual pation of a motor activity (see Rigato, Murakami, & Mainen, fields (see Karnath, 2015). These patients, who are said to 2014; Siegel, Buschman, & Miller, 2015), but those in the suffer from object-based contralateral neglect, fail to respond dorsolateral prefrontal association cortex tend to fire first. to the left side of objects (e.g., the left hand of a statue) even The response properties of dorsolateral prefrontal when the objects are presented horizontally or upside down neurons suggest that decisions to initiate voluntary move- (see Adair & Barrett, 2008). ments may be made in this area of cortex, but these deci- As you will recall, failure to perceive an object con- sions depend on critical interactions with posterior parietal sciously does not necessarily mean the object is not cortex and other areas of frontal cortex (Lee, Seo, & Jung, perceived. Indeed, two types of evidence suggest that 2012; Ptak, Schnider, & Fellrath, 2017). information about objects that are not noticed by patients with contralateral neglect may be unconsciously perceived Figure 8.3 The major cortical input and output pathways of the ­dorsolateral (see Jerath & Crawford, 2014). First, when prefrontal association cortex. Shown are the lateral surface of the left objects were repeatedly presented in the ­hemisphere and the medial surface of the right hemisphere. Not shown are the same location to the left of patients with major projections back from dorsolateral prefrontal cortex to posterior parietal cortex. contralateral neglect, they tended to look more in that general direction on future Areas of Posterior parietal secondary association cortex trials, although they were unaware of the motor objects (Geng & Behrmann, 2002). Second, cortex patients could more readily identify frag- mented (partial) drawings viewed to their Dorsolateral prefrontal right if complete versions of the drawings association had previously been presented to the left, cortex where they were not consciously perceived (Vuilleumier et al., 2002). Dorsolateral Prefrontal Association Cortex LO 8.6 Explain the role of the dorsolateral prefrontal association cortex in sensorimotor function and describe the response properties of neurons in this region of Frontal cortex. eye field Primary The other large area of association cortex motor cortex that has important sensorimotor functions M08_PINE1933_11_GE_C08.indd 218 22/01/2021 11:09  The Sensorimotor System 219 & Moran, 2012). Evidence of such a function comes from Secondary Motor Cortex brain-imaging studies in which the patterns of activity in areas of secondary motor cortex have been measured while Areas of secondary motor cortex are those that receive a volunteer is either imagining his or her own performance much of their input from association cortex (i.e., poste- of a particular series of movements or planning the perfor- rior parietal cortex and dorsolateral prefrontal cortex) and mance of the same movements (see Olshansky et al., 2015; send much of their output to primary motor cortex (see Park et al., 2015). Figure 8.4). For many years, only two areas of secondary motor cortex were known: the supplementary motor area and the Mirror Neurons premotor cortex. Both of these large areas are clearly visible on LO 8.8 Describe the major features of mirror neurons the lateral surface of the frontal lobe, just anterior to the primary and explain why they have received so much motor cortex. The supplementary motor area wraps over the attention from neuroscientists. top of the frontal lobe and extends down its medial surface into the longitudinal fissure, and the premotor cortex runs in a Few discoveries have captured the interest of neurosci- strip from the supplementary motor area to the lateral fissure. entists as much as the discovery of mirror neurons (see Rizzolatti & Fogassi, 2014). Mirror neurons are neurons Identifying the Areas of Secondary that fire when an individual performs a particular goal- Motor Cortex directed movement or when they observe the same goal- directed movement performed by another. LO 8.7 Explain the general role of areas of secondary Mirror neurons were discovered in the early 1990s motor cortex. in the laboratory of Giacomo Rizzolatti (see Ferrari & The simple two-area conception of secondary motor cortex Rizzolatti, 2014). Rizzolatti and his colleagues had been has become more complex. Neuroanatomical and neuro- studying a class of macaque monkey ventral-premotor-area physiological research with monkeys has made a case for at neurons that seemed to encode for particular goal objects; least eight areas of secondary motor cortex in each ­ h emisphere, each with its own subdivisions (Nachev, Figure 8.4 Three sorts of secondary motor cortex—supplementary motor area, ­Kennard, & Husain, 2008). Although premotor cortex, and cingulate motor areas—and their output to the primary motor cortex. Shown are the lateral surface of the left hemisphere and the medial surface most of the research on second- of the right hemisphere. ary motor cortex has been done in Supplementary Cingulate monkeys, functional brain-imaging motor area motor areas studies have suggested that human secondary motor cortex has a com- parable organization (see Caminiti, Primary Innocenti, & Battaglia-Mayer, 2015). motor To qualify as secondary motor cortex cortex, an area must be appropriately Premotor connected with association and sec- cortex ondary motor areas (see Figure 8.4). Electrical stimulation of an area of sec- ondary motor cortex typically elicits complex movements, often involving both sides of the body. Neurons in an area of secondary motor cortex often become more active just prior to the initiation of a voluntary movement and continue to be active throughout the movement. In general, areas of second- ary motor cortex are thought to be involved in the programming of specific patterns of movements after taking general instructions from dor- solateral prefrontal cortex (see Pearce M08_PINE1933_11_GE_C08.indd 219 22/01/2021 11:09  220 Chapter 8 that is, these neurons fired when the monkey reached for cooperation, and imitation (see Farina, Borgnis, & Pozzo, one object (e.g., a specific toy) but not when the monkey 2020; Rizzolatti & Sinigaglia, 2016; Wood et al., 2016; but see reached for another. Then, they noticed something strange: Fitch, 2017; Kennedy-­Constantini, 2017). Some of these neurons, later termed mirror neurons, fired just Support for the idea that mirror neurons play a role as robustly when the monkey watched the experimenter in social cognition has come from demonstrations that pick up the same object but not others—see Figure 8.5. these neurons respond to the understanding of the purpose Why did the discovery of mirror neurons in the of an action, not to some superficial characteristic of the ventral premotor area create such a stir? The reason is action itself (Rizzolatti & Sinigaglia, 2016; but see Church- that they provide a possible mechanism for social cognition land, 2014). For example, mirror neurons that reacted to (knowledge of the perceptions, ideas, and intentions of the sight of an action that made a sound (e.g., cracking a others). Mapping the actions of others onto one’s own peanut) were found to respond just as robustly to the sound action repertoire might facilitate social understanding, alone—in other words, they responded fully to the particu- lar action and its goal regardless of how it was detected. Indeed, Figure 8.5 Responses of a mirror neuron of a monkey. many ventral premotor mirror neurons fire even when a monkey does not perceive the key action but just creates a mental represen- tation of it. Mirror neurons have been found in several areas of the macaque monkey frontal and parietal cortex (see Bonini & Ferrari, 2011; Giese & Rizzolatti, 2015). However, despite more than 600 published studies of “mirror systems” in humans, descriptions of individual mir- ror neurons in humans are rare Time Time Pickup Pickup (see Molenberghs, Cunnington, & Mattingley, 2012). Indeed, we A mirror neuron in the premotor cortex The same monkey mirror neuron fires of a monkey fires when the monkey when the experimenter picks up the ball. know of only one: Mukamel and picks up the ball. colleagues (2010). This is because there are few opportunities to record the firing of individual neurons in humans while con- ducting the required behavioral tests. Most of the research on human mirror neuron mecha- nisms have been functional MRI studies. Many of these stud- ies have found areas of human motor cortex that are active when a person performs, watches, or imagines a particular action (e.g., Farina, Borgnis, & Pozzo, 2020; Rizzolatti & Sinigaglia, 2016; Vogeley, 2017). There is no direct Time Time Pickup Pickup evidence that mirror neurons are responsible for these human The same monkey mirror neuron The same monkey mirror neuron ­findings—it is possible that dif- does not fire when the monkey does not fire when the experimenter picks up an object other than the ball. picks up an object other than the ball. ferent neurons in the same cortical areas contribute to the functional M08_PINE1933_11_GE_C08.indd 220 22/01/2021 11:09  The Sensorimotor System 221 MRI activity in these different conditions. However, the Conventional View of Primary Motor mirror mechanisms identified by functional MRI in humans tend to be in the same areas of cortex as those identified by Cortex Function single cell recording in macaques (Molenberghs et al., 2012). LO 8.9 Describe the conventional view of primary motor cortex function and the evidence upon which it was based. Primary Motor Cortex In 1937, Penfield and Boldrey mapped the primary motor The primary motor cortex is located in the precentral gyrus of cortex of conscious human patients during neurosurgery the frontal lobe (see Figures 8.3, 8.4, and 8.6). It is the major by applying brief, low-intensity electrical stimulations to point of convergence of cortical sensorimotor signals, and various points on the cortical surface and noting which it is the major, but not the only, point of departure of senso- part of the body moved in response to each stimulation. rimotor signals from the cerebral cortex. Understanding of They found that the stimulation of each particular cor- the function of primary motor cortex has undergone radical tical site activated a particular contralateral muscle and changes over the past two decades—see Graziano (2016). produced a simple movement. When they mapped out The following two sections describe these changes. the relation between each cortical site and the muscle that was activated by its stimulation, they found that the primary motor cortex is organized Figure 8.6 The motor homunculus: the somatotopic map of the human somatotopically—that is, according to a primary motor cortex. Electrical stimulation of various sites in the primary map of the body. The somatotopic layout motor cortex elicits simple movements in the indicated parts of the body. of the human primary motor cortex is com- Shoulder monly referred to as the motor homunculus Trunk (see Figure 8.6). Notice that most of the Elbow t d Wris Hip Han Ri le primary motor cortex is dedicated to con- t g Lit n e trolling parts of the body that are capable dl id ex M d of intricate movements, such as the hands Knee In mb u and mouth. Th k c d It is important to appreciate that each site Ne ow an Ankle r l B ye alli d in the primary motor cortex receives sensory E eb feedback from receptors in the muscles and Ey e joints that the site influences. One interesting Toes Fac exception to this general pattern of feedback Lips has been described in monkeys: Monkeys have at least two different hand areas in the Jaw primary motor cortex of each hemisphere, and one receives input from receptors in the Tongue skin rather than from receptors in the mus- cles and joints. Presumably, this latter adap- Swallowing tation facilitates stereognosis—the process of identifying objects by touch. Close your Primary eyes and explore an object with your hands; motor Central notice how stereognosis depends on a com- cortex fissure plex interplay between motor responses and the somatosensory stimulation produced by them (see Kappers, 2011). What is the function of each primary motor cortex neuron? Until recently, each neuron was thought to encode the direction of movement. The main evidence for this was the finding that each neuron in the arm area of the primary motor cortex fires maximally when the arm reaches in a particular direc- Based on Penfield, W., & Rasmussen, T. (1950). The cerebral cortex of man: a clinical study of the tion and that each neuron has a different pre- localization of function. New York, NY: Macmillan. ferred direction. M08_PINE1933_11_GE_C08.indd 221 22/01/2021 11:09  222 Chapter 8 Current View of Primary Motor The importance of the target of a movement, rather than the direction of a movement, for the function of Cortex Function primary motor cortex was also apparent in stimulation LO 8.10 Describe the current view of primary motor studies (see Graziano, 2016; Harrison & Murphy, 2014). cortex function and the evidence upon which For example, if stimulation of a particular motor cortex site it is based. caused a straight arm to bend at the elbow to a 90-degree angle, stimulation of the same site caused a tightly bent Recent efforts to map the primary motor cortex have used arm (i.e., bent past 90 degrees towards the animal’s body) a new stimulation technique—see Graziano (2016). Rather to straighten to the same 90-degree angle. In other words, than stimulating with brief pulses of current that are just the same stimulation of motor cortex can produce opposite above the threshold to produce a reaction, investigators movements depending on the starting position, but the end have used longer bursts of current (e.g., 0.5 to 1 seconds; position of the movements remains the same. Stop for a see Van Acker et al., 2014), which are more similar to the moment and consider the implications of this finding—they duration of a motor response. The results were amazing: are as important as they are counterintuitive. First, the finding Rather than eliciting the contractions of individual muscles, means that the signals from every site in the primary motor these currents elicited complex natural-looking response cortex diverge greatly, so each particular site has the ability to sequences. For example, stimulation at one site reliably get a body part (e.g., an arm) to a target location regardless of produced a feeding response: The arm reached forward, the starting position. Second, it means that the sensorimotor the hand closed as if clasping some food, the closed hand system is inherently plastic. Apparently, each location in the was brought to the mouth, and finally the mouth opened. primary motor cortex can produce the innumerable patterns These recent studies have revealed a looser somatotopic of muscle contraction and relaxation (Davidson et al., 2007) organization than was previously thought. For example, required to get a body part from any starting point to a although stimulations to the face area do tend to elicit facial specific target location. Accordingly, it has been suggested movements, those movements are complex species-typical that the primary motor cortex contains an action map (see movements (e.g., an aggressive facial expression) rather Graziano, 2016) in addition to a topographic map. than individual muscle contractions (see Ejaz, Hamada, & The neurons of the primary motor cortex play a major Diedrichsen, 2015). Also, sites that move a particular body role in initiating body movements. With an appropriate part overlap greatly with sites that move other body parts interface, could they control the movements of a machine (Sanes et al., 1995). Presumably that is why small lesions (see Georgopoulos & Carpenter, 2015)? Belle says, “Yes.” in the hand area of the primary motor cortex of humans (Scheiber, 1999) or monkeys (Scheiber & Poliakov, 1998) do not selectively disrupt the activity of a single finger. Belle: The Monkey That The conventional view that many primary motor cortex ­Controlled a Robot with Her Mind neurons are tuned to movement in a particular direction has also been challenged. In the many studies that have sup- I­n the laboratory of Miguel Nicolelis and John Chapin, a tiny owl ported this conventional view, the monkey subjects were monkey called Belle watched a series of lights on a control panel. trained to make arm movements from a central starting Belle had learned that if she moved the joystick in her right hand point so that the relation between neural firing and the direc- in the direction of a light, she would be rewarded with a drop of tion of movement could be precisely assessed. In each case, fruit juice. On this particular day, as a light flashed on the panel, each neuron fired only when the movements were made at 100 microelectrodes recorded extracellular unit activity from a particular angle. However, an alternative to the idea that neurons in Belle’s primary motor cortex. This activity moved motor neurons are coded to particular angles of movement Belle’s arm toward the light, but at the same time, the signals were analyzed by a computer, which fed the output to a labora- has come from the findings of studies in which the activity tory several hundred kilometers away, at the M ­ assachusetts of individual primary motor cortex neurons is recorded as Institute of Technology. At MIT, the signals from Belle’s brain monkeys moved about freely (see Graziano, 2016; Harrison entered the circuits of a robotic arm. On each trial, the activity & Murphy, 2014)—rather than as they performed simple, of Belle’s primary motor cortex moved her arm toward the test learned arm movements from a set starting point. The fir- light, and it moved the robotic arm in the same direction. Belle’s ing of many primary motor cortex neurons in freely moving neural signals were directing the activity of a robot. monkeys was often related to the particular end point of a movement, not to the direction of the movement. That is, if a monkey reached toward a particular location, primary Belle’s remarkable feat raised a possibility that is start- motor cortex neurons sensitive to that target location tended ing to be realized. Indeed, there has been a recent flurry of to become active regardless of the direction of the movement technological advances involving brain–computer interfaces that was needed to get from the starting point to the target. (i.e., direct communication between a computer and the M08_PINE1933_11_GE_C08.indd 222 22/01/2021 11:09  The Sensorimotor System 223 brain—usually via an array of electrodes placed in the brain). (see Bostan & Strick, 2018; Buckner, 2013). And while it For example, paralyzed patients have learned to control constitutes only 10 percent of the mass of the brain, the robotic arms with neural signals collected via multi-electrode cerebellum contains more than half of the brain’s neurons arrays implanted in the primary motor cortex (Collinger (Azevedo et al., 2009). et al., 2013; Golub et al., 2016; Pruszynski & Diedrichsen, 2015). The cerebellum receives information from primary and Brain-computer interfaces have also been used to secondary motor cortex, information about descending mitigate the effects of spinal-cord damage. For example, motor signals from brain-stem motor nuclei, and feedback in a study by Capogrosso and colleagues (2016), mon- from motor responses via the somatosensory and vestibu- keys with transected spinal cords each had a wireless lar systems. The cerebellum is thought to compare these transmitter implanted in their motor cortex to record and three sources of input and correct ongoing movements that transmit motor cortex activity. Another wireless receiver deviate from their intended course (see Bastian, 2006; Bell, positioned on their spinal cord just below the site of tran- Han, & Sawtell, 2008; Herzfeld & Shadmehr, 2014). By per- section converted that transmitted message into a pattern forming this function, it is believed to play a major role in of stimulation that elicited movement of their paralyzed limb motor learning, particularly in the learning of sequences of (Capogrosso et al., 2016). Such brain–spine-computer interfaces movements in which timing is a critical factor (see Pritchett might someday allow for significant recovery from the effects & Carey, 2014). of spinal cord damage (see Jackson, 2016). The effects of diffuse cerebellar damage on motor func- tion are devastating. The patient loses the ability to accurately E F F E C T S O F P R I M A RY M O T O R C O RT E X control the direction, force, velocity, and amplitude of move- LESIONS. Extensive damage to the human primary motor ments and the ability to adapt patterns of motor output to cortex has less effect than you might expect, given that this changing conditions. It is particularly difficult to maintain cortex is the major point of departure of motor fibers from steady postures (e.g., standing), and attempts to do so fre- the cerebral cortex. Large lesions to the primary motor cor- quently lead to tremor. There are also severe disturbances tex may disrupt a patient’s ability to move one body part in balance, gait, speech, and the control of eye movement. (e.g., one finger) independently of others (see Ebbesen & Learning new motor sequences is difficult (Thach & Bastian, Brecht, 2017), may produce astereognosia (deficits in ste- 2004). These effects of cerebellar damage suggest that the cer- reognosis), and may reduce the speed, accuracy, and force ebellum plays a major role in monitoring and adapting ongo- of a patient’s movements. Such lesions do not, however, ing patterns of movement (see Peterburs & Desmond, 2016) eliminate voluntary movement, presumably because there The functions of the cerebellum were once thought are parallel pathways that descend directly from secondary to be entirely sensorimotor, but this conventional view is and association motor areas to subcortical motor circuits no longer tenable (see Buckner, 2013; Koziol et al., 2014). without passing through primary motor cortex. Patients with cerebellar damage often display diverse sensory, cognitive, emotional, and memory deficits (see ­Sokolov, Miall, & Ivry, 2017). Also, healthy volunteers often Cerebellum and Basal display cerebellar activity during sensory, cognitive, or emotional activities. There are several competing theories Ganglia of cerebellar function (see Koziol et al., 2014), but a popular one is that the cerebellum plays an important role in learn- The cerebellum and the basal ganglia (see Figures 3.20 and ing from one’s errors and in the prediction of errors (see 3.28) are both important and highly interconnected senso- Herzfeld et al., 2018; Sokolov, Miall, & Ivry, 2017). rimotor structures (see Bostan & Strick, 2018), but neither is a major part of the pathway by which signals descend through the sensorimotor hierarchy. Instead, both the cer- Basal Ganglia ebellum and the basal ganglia interact with different levels of the sensorimotor hierarchy and, in so doing, coordinate LO 8.12 Describe the anatomy of the basal ganglia and and modulate its activities. explain the current view of their function. The basal ganglia do not contain as many neurons as the Cerebellum cerebellum, but in one sense they are more complex. Unlike the cerebellum, which is organized systematically in lobes, LO 8.11 Describe the structure and connectivity of the columns, and layers, the basal ganglia are a complex hetero- cerebellum and explain the current view of geneous collection of interconnected nuclei. cerebellar function. The anatomy of the basal ganglia suggests that, like The cerebellum’s structure and complex connectivity with the cerebellum, they perform a modulatory function (see other brain structures suggest its functional complexity Nelson & Kreitzer, 2014). They contribute few fibers to M08_PINE1933_11_GE_C08.indd 223 22/01/2021 11:09  224 Chapter 8 descending motor pathways; instead, they form neural One theory of basal ganglia sensorimotor function is loops via their numerous reciprocal connections with corti- based on its known roles in both movement and motiva- cal areas and the cerebellum (Bostan & Strick, 2018; Nelson tion (see Averbeck & Costa, 2017; Schultz, 2016). This the- & Kreitzer, 2014; Oldenburg & Sabatini, 2015). Many of the ory comprises two major assertions. The first states that cortical loops carry signals to and from the motor areas of the basal ganglia are responsible for movement vigor (see the cortex (see Nambu, 2008). Dudman & Kraukauer, 2016): the control of the speed and Theories of basal ganglia function have changed in much amplitude of movement based on motivational ­factors. For the same way that theories of cerebellar function have changed. example, the basal ganglia might enable a concert pianist to The traditional view of the basal ganglia was that they, like the play a particular piece with more or less vigor. The second cerebellum, play a role in the modulation of motor output. Now, assertion is that movement not only involves the execu- the basal ganglia are thought to also be involved in a variety tion of actions but also requires that we actively suppress of cognitive functions (see Eisinger et al., 2018; Hikosaka et al., motor activity that would otherwise be inappropriate or 2014; Lim, Fiez, & Holt, 2014; Rektor et al., 2015) and in many unhealthy. For example, we have to suppress our tendency aspects of motivation (see Bostan & Strick, 2018). The basal to display inappropriate yawning or scratching at social ganglia have also been shown to participate in learning. For gatherings; we also need to suppress unwanted move- example, they play a role in habit learning, a type of learning ments generated by the ongoing spontaneous activity of that is usually acquired gradually, trial-by-trial (see Ashby, our muscles (e.g., tremor, twitching, coughing). When such Turner, & Horovitz, 2010), and in classical conditioning (see movement inhibition fails, symptoms of a neurological or Stephenson-Jones et al., 2016). psychiatric disorder can emerge (see Duque et al., 2017). Scan Your Brain Now that you have learned about the sensorimotor pathways, ­opposite to the side of a brain lesion in the absence of this is a good place for you to pause to scan your brain to e ­ valuate simple sensory or motor deficits. your knowledge by completing the following s­ tatements. The 6. The supplementary motor area and premotor cortex are correct answers are provided at the end of the exercise. Before part of the _______ _______ cortex that is involved in proceeding, review material related to your incorrect answers ­programming patterns of movements. and omissions. 7. _______ are neurons that fire when an individual ­ erforms a particular goal-directed hand movement or p 1. The _______ _______ association cortex provides when they observe the same goal-directed movement i­mportant spatial information and helps direct attention performed by another. to external stimuli. 8. The somatotopic layout of the human primary cortex is also 2. _______ movements are normally not affected by sensory known as the _______ _______. feedback. 9. The _______ is involved in motor learning and the 3. Motor learning, such as riding a bike, begins with responses t­emporal association of motor actions. As such, under conscious control, but with practice these are ­damage to this area can cause detrimental effects on adjusted by _______ feedback without conscious regulation. posture, gait, speech, and balance. 4. _______ is a disorder of voluntary movement that cannot 10. Recent views of the function of the basal ganglia be explained by paralysis; rather, it is attributed to the s­ uggest that they are involved in various cognitive inability to perform motor movements when instructed to ­functions including _______ learning. do so. (9) cerebellum, (10) habit. 5. _______ _______, a striking consequence of posterior (6) secondary motor, (7) Mirror neurons, (8) motor homunculus, parietal cortex damage, is a disturbance of a patient’s (3) sensory, (4) Apraxia, (5) Contralateral neglect, ability to respond to stimuli on the side of the body Scan Your Brain answers: (1) posterior parietal, (2) Ballistic, pathways, and two descend in the ventromedial region of the Descending Motor spinal cord—collectively known as the ventromedial motor Pathways pathways. Signals conducted over these pathways act together in the control of voluntary movement (see Iwaniuk & Whishaw, Neural signals are conducted from the primary motor cortex 2000). Like a large company, the sensorimotor system does not to the motor neurons of the spinal cord over four different work well unless there are good lines of communication from pathways. Two pathways descend in the dorsolateral region of the executive level (the cortex) to the office personnel (the the spinal cord—collectively known as the dorsolateral motor spinal motor circuits) and workers (the muscles). M08_PINE1933_11_GE_C08.indd 224 22/01/2021 11:09  The Sensorimotor System 225 The Two Dorsolateral Motor In contrast, the dorsolateral tracts control the movements of the limbs (see Ruder & Arber, 2019). Pathways and the Two Ventromedial Motor Pathways LO 8.13 Compare and contrast the two dorsolateral Sensorimotor Spinal motor pathways and the two ventromedial motor pathways. Circuits The descending dorsolateral and ventromedial motor path- We have descended the sensorimotor hierarchy to its low- ways are similar in that each is composed of two major tracts, est level: the spinal circuits and the muscles they control. one whose axons descend directly to the spinal cord and Psychologists, including us, tend to be brain-oriented, another whose axons synapse in the brain stem on neurons and they often think of the spinal cord motor circuits as that in turn descend to the spinal cord. However, the dorsolateral mere cables that carry instructions from the brain to the tracts differ from the ventromedial tracts in two major respects: muscles. If you think this way, you will be surprised: The motor circuits of the spinal cord show considerable com- The ventromedial tracts are much more diffuse. Many plexity in their functioning, independent of signals from of their axons innervate interneurons on both sides the brain (see Dasen, 2017; Giszter, 2015; Kiehn, 2016; Ruder of the spinal gray matter and in several different seg- & Arber, 2019). Again, the business metaphor helps put this ments, whereas the axons of the dorsolateral tracts in perspective: Can the office managers (spinal circuits) terminate in the contralateral half of one spinal cord and workers (muscles) of a company function effectively segment, sometimes directly on a motor neuron. when all of the executives are at a convention in Hawaii? The motor neurons activated by the ventromedial tracts Of course they can. project to proximal muscles of the trunk and limbs (e.g., shoulder muscles), whereas the motor neurons acti- Muscles vated by the dorsolateral tracts project to distal muscles (e.g., finger muscles). LO 8.14 Describe the components of a motor unit and distinguish between the different types of Because all four of the descending motor tracts originate muscles. in the cerebral cortex, all are presumed to mediate volun- tary movement; however, major differences in their routes Motor units are the smallest units of motor activity. Each and destinations suggest that they have different functions. motor unit comprises a single motor neuron and all of the This difference was first demonstrated in an experiment on individual skeletal muscle fibers that it innervates (see monkeys by Lawrence and Kuypers. ­Figure 8.7). When the motor neuron fires, all the muscle In their experiment, Lawrence and Kuypers (1968) made fibers of its unit contract together. Motor units differ appre- complete transections of the dorsolateral tracts in monkeys. ciably in the number of muscle fibers they contain; the The monkeys could stand, walk, and climb after this transec- units with the fewest fibers—those of the fingers and face—­ tion, but when they were sitting, their arms hung limply by permit the highest degree of selective motor control. their sides (remember that monkeys normally use their arms A skeletal muscle comprises hundreds of thousands of for standing and walking). In those few instances in which threadlike muscle fibers bound together in a tough mem- the monkeys did use an arm for reaching, they used it like a brane and attached to a bone by a tendon. Acetylcholine, which rubber-handled rake—throwing it out from the shoulder and is released by motor neurons at neuromuscular junctions, using it to draw small objects of interest back along the floor. activates the motor end-plate on each muscle fiber and The other group of monkeys in their experiment had causes the fiber to contract. Contraction is the only method complete transections of their ventromedial tracts. In con- that muscles have for generating force, thus, any muscle can trast to the first group, these subjects had severe postural generate force in only one direction. All of the motor neu- abnormalities: They had great difficulty walking or sitting. rons that innervate the fibers of a single muscle are called If they did manage to sit or stand without clinging to the its motor pool. bars of their cages, the slightest disturbance, such as a loud Although it is an oversimplification (see Gollnick & noise, frequently made them fall. Hodgson, 1986), skeletal muscle fibers are often considered What do these experiments tell us about the roles of to be of two basic types: fast and slow. Fast muscle fibers, as the various descending sensorimotor tracts in the control you might guess, are those that contract and relax quickly. of primate movement? They suggest that the ventromedial Although they are capable of generating great force, they tracts are involved in the control of posture and whole-body fatigue quickly because they are poorly vascularized (have movements (e.g., walking, climbing) and that they can exert few blood vessels, which gives them a pale color). In con- control over the limb movements involved in such activities. trast, slow muscle fibers, although slower and weaker, are M08_PINE1933_11_GE_C08.indd 225 22/01/2021 11:09  226 Chapter 8 elastic, rather than inflexible and cablelike. If you think of Figure 8.7 An electron micrograph of a motor unit: a motor neuron (pink) and the muscle fibers it innervates. an increase in muscle tension as analogous to an increase in the tension of an elastic band joining two bones, you will appreciate that muscle contraction can be of two types. Activation of a muscle can increase the tension that it exerts on two bones without shortening and pull- ing them togethe