The output map of the primate motor cortex

The outputmap of the primate motor cortex Roger

What is 'represented' in the primate motor cortex? Most approaches have defined the output map of the cortex rather than giving any clear answers as to functional representation. This results in part from the artificial nature of the electrical stimuli used to map the outputs. The 'spike-triggered averaging" technique avoids this problem and has demonstrated that single cortical neurones facilitate functional subsets of muscles in the monkey forelimb. The output map revealed by this approach shows that clusters of output neurones facilitate the same muscle, and each muscle is represented many times over in the cortex. The overlapping representations of different muscles may subserve the control of the complex muscle synergies that underlie voluntary movement.

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central nervous system knows nothing of muscles, it RogerLemonisat the only knows movements'. Phillips 9 has argued strongly Departmentof that 'muscles versus movements' is an artificial Anatomy, Cambridge antithesis and that electrical stimulation methods are University, CambridgeCB23DY, not suitable to resolve it. UK. Different types of motor cortex map Since section of the pyramidal tract causes profound changes in the motor map 1°, and since electrical stimulation is generally thought to activate the lamina V neurones that give rise to this tract, most of the debate on representation in the motor cortex has concerned its output map. But there are other important maps within area 4: these include an input map of afferents arriving over cortico-cortical and subcortical pathways, and including direct somatosensory feedback from the moving limb 11'12. These inputs select intracortical circuits that can operate the cortical outputs to construct the complex patterns of muscular activity underlying voluntary movement. This operation is represented as a series of functional maps within the motor cortex. The relative simplicity of movements elicited by cortical stimulation suggests that these functional maps are considerably more complex than the output map itself.

Cortical localization of function is one of the major tenets of modern neuroscience. Although functional localization is now usually illustrated by reference to visual cortical areas, experimental investigation actually began in the motor cortex, when, in 1870, Fritsch and Hitzig demonstrated that galvanic electrical stimulation of dog cortex evoked movements of the contralateral limbs. The representation of movements within the precentral motor cortex (area 4 of Brodmann) was first systematically mapped by Leyton and Sherrington 1. The pictorial summary of Detecting the cortical output their experiments (Fig. 1) shows an orderly represenThe coarse structure of the output map, as defined tation of the movements elicited in different parts of by classical stimulation studies, consists of distinct the body by cortical stimulation, a finding since regions from which movements of different body parts replicated in a great many studies (see Refs 2 and 3 (face, arm, hand, etc.) can be evoked. Most of the for reviews). However, recent investigations into the disagreement has concerned the fine structure of this fine structure of this map argue Toes Sulcus strongly against a purely somatotopic representation of muscles in the motor cortex output and provide some clues as to how the cortical output controls the different subsets of muscles that are used in all but the simplest of voluntary movements. These EIb new findings have been revealed Wri~ by careful use of intracortical stimulation in conscious animals3-6, Fingers and by the use of 'spike-triggered thumb averaging', a sophisticated method of examining the cortical output that completely avoids the disruptive effects of electrical stimuli upon the brain 7,s. Two closely linked problems have clouded the question of functional representation in the motor Ea cortex: the action of electrical stimuli on the cortex; and the issue of whether 'muscles or movements' are 'represented' at the cortical Opening cords , u,-,.,, level. This knotty problem arose Mastication of jaw when Beevor (and many since) made a literal interpretation of Fig. 1. Summary diagram of the experiments performed by Leyton and Sherrington ~ on the metaphor used by Hughlings movements of different parts of the body eficited by electrical stimulation of the cortex of the Jackson 'To speak figuratively, the chimpanzee. The motor area is indicated by stippling. TINS, Vol. 11, No. 11, 1988

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animals up to long trains of repetitive stimuli, with strengths of up to 60 ~tA, in sedated animals. i ..... .... .. , ,'. Small wonder that the resulting maps are different! . . ... . .. . ... . . . ~, ,, ,. . :'~ ~, -o'" ""; Sa Wp-"Wf S a : : ! .......... , ; • , : Nevertheless it is more im• ............... . ' 0 , • .. . . . . . . . . . . o, ,, .~ . / " ', ' ' ~ ....... :r Sb' ' • _* ',** Sb: portant now than at any other time to understand the action of ...i ....... ..'\ •' ....!.. "Sh '-$ Sa"FfTa Ws We-We ",Sa' *' " electrical stimuli upon the cortex. -TT", " ") \ i : This is because of the develop"::'"" medial!""-'' ::::" ....: "" ~ ~ " "'':; "'-) '! '" . . . . . . . . . " . / (We "'(,. -' : " ment of non-invasive, trans-cranial f ( i . . . . . : (,Ta FeLFf" " WS--)F , ' ." stimulation of the human brain 17. / i !,.--'" , ./:' For this technique to be of real 1ram . ,:F,Ta 11W s FeWe T. Ws . diagnostic value, it is essential r o s t . . , •• "' k : to understand its effect upon the "" '" ~ ! am 5 : EfWs Ef--Ws~ e-,=. brain. Several animal studies have / ICMS -- 10 ....... ~,f ............ demonstrated that a large proporstrength --- 25 • FCR+ECR tion of the pyramidal tract neurones excited by intracortical stimuli are (pA) . . . . . 40 Fig. 2. Multiple representation of (A) muscles and (B) movements evoked from motor cortex by not excited directly, but indirectly ICMS in a conscious macaque monkey• Parts of the map overlapping the central sulcus indicate or trans-synaptically 2'6' is, ]9. There buried areas in its rostral bank. (A) The surface projection of the representation of a single wrist is also some evidence for indirect muscle. Repetitive ICMS was delivered within lamina V; the contours enclose areas from which activation of pyramidal tract neuactivity m extensor carpi radialis (ECR) was evoked by stimulus trains of S, 10, 25 and 40#A. Note rones by magnetic stimulation of the discontinuity of the lowest threshold area, and the large areas occupied by the l OlzA and 251zA the human brain 2°. Intracortical maps. (B) Projection of the movements observed from the same sites in lamina V onto the ECR stimuli are thought to activate contour map. Wrist extension (We) occurs only on stimulation within or immediately adjacent to fibres afferent to the pyramidal the two low-threshold sites. At all other sites ECR is activated as one of a set of stabilizing muscles tract neurones; these input fibres during another primary movement. El, elbow flexion; Fe, finger extension; F~, finger flexion," Ta, thumb adduction; Sa, Sb, shoulder adduction or abduction; Wf, wrist flexion; Wp, pronation; W~, (which far outnumber those of supination. The filled circles ( e ) show all locations from which co-activation of ECR and FCR (flexor the pyramidal tract axons) exert powerful excitatory effects upon carpi radialis) was obtained. (Taken, with permission,from Ref. 3.) the pyramidal tract neurones. output map. Differences as to its form and organiz- Whereas the trans-synaptic spread of excitation that ation have resulted chiefly from investigators select- results from single intracortical shocks is probably ing different levels at which to monitor the output. restricted by the local organization of synaptic input 1`~, These output levels were chosen to suit the purpose repetitive stimuli probably recruit much larger of the experiment: to detect the full extent of the numbers of pyramidal tract neurones 6, some of which output from a particular cortical zone, or to look for may lie at some distance from the stimulating electrode the dominant motor effect from that zone (see Ref. 3 (600 ~tm for single ICMS of 4 ~tA in lamina VlS). Indirect for a review). Thus, some have chosen as the most activation of pyramidal tract neurones by electrical sensitive indicator of this output the production of stimuli means that to some extent the resulting motor postsynaptic potentials in spinal motoneurones2; effects reflect the organization of inputs to the others have looked for changes in the activity of single pyramidal tract neurones, rather than the output of the motor units 13, or of multi-unit EMG (electro- pyramidal tract neurones themselves and places new myogram) 5'6'~4'15. Finally, many studies have chosen emphasis on the need for studies on the input pathways the production of a detectable movement by cortical to motor cortex. Sherrington pointed out 'the profound stimulation 4'x5. This is probably the crudest but difference existing between the production of the finer movements of the limb in volition on the one hand and arguably most relevant indicator of cortical output. by experimental stimulation of the cortex on the other'. The artificial nature of electrical stimulation makes it difficult for this approach to yield further insights into The action of electrical stimuli Further disagreements about the output map are the functions of motor cortex. Electrical stimulation due to differences in the type of electrical stimulation cannot mimic but does disrupt the progress of used. The classical work of Penfield (in man), and of voluntary movement. Woolsey, was done using stimulation of the cortical surface with alternating current. Phillips 2 developed E m e r g e n t features of the output map Notwithstanding the limitations of stimulation the use of single, surface anodal stimuli for direct excitation of pyramidal tract neurones. Asanuma 16 methods, they have provided important clues about introduced the technique of intracortical microstimu- the features of the fine, intra-areal output map. The lation (ICMS) through the tip of a metal micro- first feature is the multiple representation of cortical electrode, and this technique has since been widely output to single motoneurones and individual muscles; used in conscious animals. The last meeting of the these different representations converge upon the Society for Neuroscience in New Orleans boasted motoneurones of their target muscle. Second, cortical papers from different laboratories studying the effects outputs to different motoneurones or muscles are of stimulating the primate motor cortex with anything found to overlap each other extensively. Single from single intracortical shocks of 2.5 ~tA in conscious motoneurones can be activated from relatively large SU|CUS

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areas of the cortex, and these areas are often discontinuous 2,13; the same holds true for activation of single muscles or movements4'5'1°. Figure 2A, taken from Humphrey's study3, shows how one muscle (extensor carpi radialis, ECR) can be activated by ICMS from an extensive cortical area. The lowest threshold points are clearly discontinuous. Wrist movements could also be evoked from extensive and discontinuous sites (Fig. 2B); the sites from which the muscle could be activated formed a much larger area than that found for wrist extension movements. The large areas involved [up to 7 mm2 (Refs 2, 13)] mean that a considerable degree of overlap must exist between the outputs to different muscles for all of these to be represented within the confines of the primary motor cortex: in the example shown in Fig. 2B, ECR was coactivated with muscles subserving movements other than wrist extension. N e w approaches to the map A further property of the cortical output divergence - became strikingly apparent when the intraspinal branching pattern of corticospinal axons A

was revealed21'22. These studies showed single axons branching profusely within different motor nuclei (Fig. 3B) and stressed the importance of the intraspinal connections in determining the motor consequences of a given cortical output, and thereby the shape of the cortical map. The introduction of the spike-triggered averaging technique by Fetz and his colleagues has made it possible to identify, in the conscious monkey, both the cells of origin of the direct, cortico-motoneuronal (CM) projection (which is found almost exclusively in primates) and their target muscles 7's. This method involves averaging the rectified EMG recorded from different limb muscles with respect to the discharges of a single cortical neurone. A direct, functional linkage between the neurone and the motoneurones of the muscle is indicated by the presence of a transient post-spike facilitation of EMG activity in the resulting average, such as that produced in the EMG of abductor pollicis brevis (AbPB) in Fig. 3A. This method uses the natural, movement-related discharge of CM cells recorded in awake, behaving monkeys, and is thus ideally suited to the study of the natural

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Fig. 3. (A) Distribution of post-spike facilitation from single CM cells to muscles of the hand and forearm in the monkey. Spike-triggered averages of EMG recorded concurrently from ten muscles and averaged with respect to 10 000 spikes from a pyramidal tract neurone, which discharged at time zero. All data were recorded while the monkey performed a precision grip task between thumb and index finger. Asterisks indicate averages with clear effects: only three of the muscles (AbPB, FPB and AdP) show definite post-spike facilitation. (B) Schematic horizontal section, at the level indicated by the arrow in (C), through the lower cervical cord showing a relatively restricted output from the axon of a single CM cell running in the lateral corticospinal tract (LCST), and with collaterals contacting motoneurone cell columns innervating two thumb muscles (FPB and AbPB), but not EDC, ECR or FCU. (D) Post-stimulus averages of EMG activity made with respect to single ICMS pulses (strength IO I~A) applied through the microelectrode at the site at which the pyramidal tract neurone in (A) was recorded. A complex response (facilitation followed by suppression) is seen in five muscles (AbPB, FPB, AdP, 1DI and AbDM), while FCU shows only suppression. (E) Responses to repetitive IC/VlSstimuli (ten shocks at 300 Hz, strength 7 tzA) at the same site. Seven muscles show responses. Abbreviations: (intrinsic hand muscles) AbPB and FPB, abductor and flexor polficis brevis; AdP, adductor pollicis; 1DI and 2DI, first and second dorsal interosseous; AbDM, abductor digiti minimi; (forearm muscles) FDS, flexor digitorum superficialis; FCU, flexor carpi ulnaris; AbPL, abductor pollicis Iongus; ED, extensor digitorum communis. (Taken, with permission, from Ref. 25 and Lemon, R., unpublished observations.) TINS, Vol. 11, No. 11, 1988

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Fig. 4. Organization of cortico-motoneuronal projections -0 * ..'o-'; © to hand and forearm muscles in the monkey. (A) Simpfified ~r ~r diagram of CM influences on wrist extensor and flexor muscles. Some CM cells facilitate agonist muscles with no effect on antagonists (a, c). Others facilitate agonist muscles (extensor motoneurone pools) and simultaneously Area3 Anterior Bank Convexity suppress antagonist musdes (flexor pools) via a reciprocal 4 0 4mm inhibitory pathway (b, e, f), or produce suppression alone s (d). The clustering of cells with common 'muscle fields" is also indicated. (Taken, with permission, from Ref. 23.) (B-E) Multiple representation and overlapping representation of intrinsic hand muscles. (B) Distribution of CM neurones that produced post-spike facilitation in the EMG of AbPB, AdP (abductor and adductor pollicis) and 1DI (first dorsal interosseous); cell locations are plotted on an unfolded map of the precentral gyrus. The unfolding is illustrated in (B) and (C). (C) shows the surface topography of microelectrode penetrations, marked by dots. The area investigated is indicated by the rectangle abcdef. (D) represents a sagittal section taken between the arrows. The gyrus was unfolded along lamina V, marked by the presence of Betz cells (dots in D). In the unfolded map, the lines a-d and b--e represent the bottom and top of the sulcus, respectively. (E) shows the overlap between CM cells projecting to the three muscles. Large triangles indicate CM cells facilitating more than one of the three muscles (Lemon, R., unpublished observations).

function of the cortex and avoids the use of electrical stimulation. This technique has provided further valuable insights into the output map: it has shown that most CM cells facilitate activity in more than one muscle. Each CM cell appears to have its own special 'muscle field'; it projects to a particular set of muscles, with each muscle receiving a different amount of facilitation. In the example shown in Fig. 3A, the CM cell strongly facilitates both the short abductor and flexor of the thumb (AbPB and FPB, respectively), and has a weaker effect upon the adductor (AdP). Many of the CM cells that project to forearm muscle groups are organized in a reciprocal fashion, facilitating extensors and inhibiting flexors or vice versaa'23'24; this arrangement is illustrated in Fig. 4A. There are no reports of a single CM cell facilitating functional antagonistic muscles. The CM projection to the muscles of the hand, and particularly that to the intrinsic thumb muscles, shows a relatively more restricted projection pattern than in the forearTnS'24'25: most of the CM cells we studied produced post-spike facilitation in only 2-3 of ten muscles acting on the fingers. This focused pattern may subserve the fractionation of hand muscle activity that is so characteristic of the primate species 26. But the divergent output from individual CM cells revealed by spike-triggered averaging makes it 504

unlikely that either single cells or groups of cells in clusters or columns are organized in terms of controlling single muscles, and at least some of the striking overlap of outputs to different muscles is explained by divergent effects from single neurones. The strength of synaptic connections from individual CM cells can be estimated by measuring the amplitude of the peaks found in cross-correlations of activity in a single CM cell and in a single motor unit of the target muscle 27. Most of these connections appear to be relatively weak (the largest unitary CM EPSPs are probably about 100-200 ~tV) and confirm that convergence of excitatory effects from many CM cells would be required to bring the target motoneurones to discharge. The CM cells that project to a given muscle appear to be distributed over a large cortical area: those that project to three different intrinsic hand muscles are shown in Fig. 4B; the overlap in the projections to these three muscles is almost complete (Fig. 4E). Cells that project to a given muscle are often found in clusters 6'23 in which neighbouring neurones share the same target muscle, although they may facilitate it to different degrees (Fig. 3A, 4A). Having revealed the organization of CM output by spike-triggered averaging, one can then compare this organization with that produced by the delivery of single pulse ICMS through the recording TINS, Vol. 11, No. 11, 1988

microelectrode 23. The existence of clusters of CM tation of different muscles within a given cortical zone Acknowledgements cells with common target muscles is confirmed by the may make kinaesiological sense3'25: there will be a Work in the author's observation that post-stimulus facilitation is usually dominant output from that zone combined with other laboratory is much stronger than the post-spike effects from single subtle facilitatory and inhibitory changes that occur in supported by the CM cells recorded at the same cortical site. Thus in other, functionally related muscles. Cortical outputs MRC, The National Fig. 3 the post-spike facilitation of the thumb abductor to both intrinsic hand and long forearm muscles are Fund for Research into Crippling (AbPB) produced by the CM cell (Fig. 3A) is 40% of especially interesting25; these two muscle groups Diseasesandthe East the background EMG level; that produced by single have to work in a highly coordinated way in order to Anglian RHA. I pulse ICMS is 162% (Fig. 3D). produce stable movements and postures with what is acknowledge the Lemon et al. 6 compared post-spike and post- an inherently unstable mechanism - the multi- collaboration of Ray stimulus effects in averages of EMG recorded from up articulate hand. Muir, GeertMantel However, it seems unlikely that single neurones or and EvertBuys, and to ten different hand and forearm muscles while monkeys performed a precision grip task. Comparison groups of neurones are coding individual movements. the useful comments of the muscle fields of neighbouring CM cells showed Georgopoulos has demonstrated that a single neurone of EberhardFetz and that although they may share a common muscle, their can be active during many different reaching Donald Humphrey. muscle fields are not identical. This seems to be movements 2s. It is more likely that the output map is Rosalyn Cummings particularly true within the hand area of the motor called upon by cortico-cortical and subcortical inputs provided excellent technical assistance. cortex, which, as Fig. 4 shows, is characterized by a to produce a certain muscle grouping or synergy, and rather heterogeneous representation of the intrinsic this synergy may be used in the production of some hand muscles. Within this area, single pulse ICMS of movements but not others. Cortico-motoneuronal 5-10 ~tA facilitated more muscles than did single CM cells are not active during all movements in which cells sampled at the same site [for the site examined their target muscles are used 7'26. This dissociation of in Fig. 3A and 3D, two additional muscles, first dorsal cortical cell and muscle activity has also been found for interosseous (1DI) and abductor digiti minimi pyramidal tract neurones active during periods when (AbDM), were facilitated by ICMS and another (flexor their presumptive target muscles are co-contracted carpi ulnaris, FCU) was suppressed]. This approach with their antagonists, but not when the muscles are also revealed that many of the effects produced by used in a reciprocal pattern of contraction 14. These single-pulse ICMS involve suppression of EMG results hint that some degree of task specificity is activity (see, for example, the averages from AbPB, represented in a functional map within motor cortex. FPB, and FCU in Fig. 3D). These effects would not, Spike-triggered averaging allows us to investigate of course, be detected if the cortex were mapped the exciting possibility that the activity of corticosolely in terms of evoked movements ~. motoneuronal cells codes for the amount of muscle ICMS with repetitive stimuli (Fig. 3E) usually activity required in a group of synergistic muscles, facilitates more muscles than observed with either and that this code is expressed via the specific spike-triggered averaging or single-pulse ICMS 5'6'z~. functional connections that the output cell makes with This result presumably reflects the spread of the spinal machinery. These experiments should excitation within the cortex stirred up by trains of reveal how functional maps in the motor cortex use its intracortical stimuli19; the spread of excitation will output connectivity for the production of complex depend on the length of the train. The corticofugal voluntary movements. volleys that result are presumably still further elaborated by temporal and spatial facilitation within Selected references the spinal cord. This elaboration is clearly an 1 Sherrington, C. S. (1947) The Integrative Action of the important feature of the cortical output, and especially Nervous System (2nd edn), Cambridge University Press so in animals lacking a direct CM projection. Because 2 Phillips, C. G. and Porter, R. (1977) Corticospinal Neurones: Their Role in Movement Academic Press of facilitation at the cortical level, repetitive ICMS is 3 Humphrey, D. R. (1986) Fed. Proc. 45, 2687-2699 not the best means of investigating the fine structure 4 Kwan, H. C., MacKay, W. A., Murphy, J. T. and Wong, Y. C of motor cortex output; on the other hand, spike(1978) J. Neurophysiol. 41, 1120-1131 triggered averaging reveals mainly monosynaptic 5 Cheney, P. D. and Fetz, E. E. (1985) J. Neurophysiol. 53, influences 7'8 and is unable to reveal the cortical output 786-804 6 Lemon, R. N., Muir, R. B. and Mantel, G. W. H. (1987) Exp. that flows over interneuronal pathways.

Functional employment of the output map All recent studies suggest that the output map of the primate motor cortex is not an orderly, topographic representation of the body's musculature. As Humphrey3 has pointed out, some of the current maps vindicate the original views of Hughlings Jackson who envisaged overlapping representations of different muscles to subserve the complex synergies that make up voluntary movements. According to this view, the representation of proximal versus distal arm muscles might be thought of as subserving a single movement synergy, such as stabilizing the arm in order that a precision finger movement might be executed, rather than for the execution of separate elbow or finger movements. The divergent output from single neurones, and the overlapping represenTINS, Vol. 11, No. 11, 1988

Brain Res. 66, 6 2 1 4 3 7 7 Fetz, E. E. and Cheney, P, D. (1980) J. Neurophysiol. 44, 751-772 8 Lemon, R. N., Mantel, G. W. H. and Muir, R. B. (1986) J. Physiol. (London) 381,497-527 9 Phillips, C. G. (1975) Can. J. Neurol. Sci. 2, 209-218 10 Mitz, A. R. and Humphrey, D. R. (1986) Neurosci. Lett. 64, 59-64 11 Wong, Y. C., Kwan, H. C., MacKay, W. ~. and Murphy, J. T. (1978) J. Neurophysiol. 41, 1107-1119 12 Lemon, R. N. (1981) J. Physiol. (London) 311,497-519 13 Andersen, P., Hagan, P. J., Phillips, C. G. and Powell, T. P. S. (1975) Proc. R. Soc. London Set. B 188, 31-60 14 Humphrey, D. R. and Reed, D. J. (1983) in Motor Control Mechanisms in Health and Disease (Desmedt, J., ed.), pp. 347-372, Raven Press 15 Huang, C-S., Sirisko, M. A., Hiraba, H., Murray, G. M. and Sessle, B. J. (1988) J. Neurophysiol. 59, 796-818 16 Asanuma, H. and Sakata, H. (1967) J. Neurophysiol. 30, 35-54 17 Merton, P. A. and Morton, H. B. (1980) Nature 285, 227

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18 Asanuma, H. and Ros6n, I. (1973) Exp. Brain Res. 16, 507-520 19 Jankowska, E., Padel, Y. and Tanaka, R. (1975) J. Physiol. (London) 249, 617-636 20 Day, B. L., Dick, J. P. R., Marsden, C. D. and Thompson, P. D. (1986) J. Physiol. (London) 378, 36P 21 Shinoda, Y., Yokota, J, I. and Futami, T. (1981) Neurosci. Left. 23, 7-12 22 Lawrence, D. G., Porter, R. and Redman, S. J. (1985) J. Comp. Neurol. 232,499-510

23 Cheney, P. D., Fetz, E. E. and Palmer, S. S. (1985) J. Neurophysiol. 53,805-820 24 Kasser, R. J. and Cheney, P. D. (1985) J. Neurophysiol. 53, 959-978 25 Buys, E. J., Lemon, R. N., Mantel, G. W. H. and Muir, R. B. (1986) J. Physiol. (London)381, 529-549 26 Muir, R. B. and Lemon, R. N. (1983) Brain Res. 261,312-316 27 Mantel, G. W. H, and Lemon, R. N. (1987) Neurosci. Left. 77, 113-118 28 Georgopoulos, A. P., Schwartz, A. B. and Kettner, R. E. (1986) Science 233, 1416-1419 i

The commandhypothesis:a new view using an old example J a m e s L. L a r i m e r

JamesL. Lanmer ts at the Department of Zoology, The University of Texas, Austin, TX78712, USA.

The interneurons that underlie abdominal flexion and extension behaviors in crustaceans were among the first to be called command neurons. They fit the original operational definition as cells that produce a welldefined movement or behavior when stimulated. Many examples of these cells are now known to influence behaviors throughout the animal kingdom. The early observation that stimulation of a single command neuron in a crustacean was sufficient to generate an apparently complete behavior led to the erroneous belief that one neuron might be responsible for one behavior. We now know that the strong stimulation of one command element is sufficient to recruit synaptically a group of similar neurons. In addition to the synaptic recruitment of agonists there is also a synaptic inhibition of their antagonists, resulting in what appears to be a complete behavior with reciprocity. Importantly, there is also evidence for the operation of similar functional groups in behaving animals. During animal-initiated behavior, each neuron in the functional group apparently makes only a minor contribution to the total motor ou~)ut with the result that no single neuron in the group is necessary to generate the behavior. I f the necessity criterion is a requirement to define a command neuron, then abdominal positioning interneurons can no longer be considered command neurons. Instead, they are cells with lesser roles, perhaps command elements in larger command systems. In spite of their diminished status, command elements occupy key positions in this and other motor systems. It has been known for many years that the stimulation of one or a few selected neurons, particularly from the nervous systems of invertebrates, can evoke specific behaviors 1. The term 'command fiber' was first introduced by Wiersma and Ikeda 2 to describe the small bundles of axons which, when dissected from the interganglionic connectives and stimulated, controlled the rhythmic beating of the abdominal appendages or swimmerets in crayfish. Similar behaviorevoking neurons were soon found in other invertebrates, particularly in molluscs and insects, and CNS centers with similar functions have also been described in the vertebrates. This important discovery clearly stirred the imagination of neurobiologists and encouraged them to believe that the neural basis of animal movements could be understood in detail. The early functional definition of a command fiber was broad, so that almost any neuron seemed to qualify as a command neuron if it released a

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movement when stimulated. However, at the same time there was a growing dissatisfaction with the broad term 'command fiber'. Some asked, 'Couldn't simple sensory neurons be incorrectly classified as command fibers if they evoked a motor output? Do these so-called command neurons actually function in behaving animals? Doesn't the name "command" imply a rigorous hierarchical system? How can we imply this when the underlying neural organization of command systems is unknown?' These and similar considerations led Kupfermann and Weiss to offer a rigorous definition of the term 'command neuron' and to suggest equally rigorous intracellular methods for studying these cells 3. We will discuss their proposals and definitions below. T h e r o l e of crustacean preparations in the

command concept In the first decade after command fibers were proposed, two behaviors in crustaceans received intensive study, abdominal positioning and swimmeret beating 4. Much of our early understanding of command neurons came from these studies. During the present decade these two systems have been examined extensively using intracellular and dyefilling methods (Fig. 1). Crustacean abdominal positioning behavior was considered advantageous because the major movements - flexion and extension - are controlled by separate ganglionic roots, and each of the six flexion and extension motor neurons in each root is identifiable from its impulse ampfitude (Fig. 1). We will briefly summarize some of the early ideas about command neurons, and afterwards turn to the more recent results obtained from crustaceans.

Early concepts The earliest studies showed that there were many neurons in various animals that could function as command neurons. With any preparation, several of these command neurons appeared to produce the same general type of movement, e.g. abdominal flexion, yet each was unique. The cells were identifiable: their axons were encountered repeatedly in the same location in the interganglionic connectives and their stimulation produced movements with unique attributes. These findings led to the belief among some workers that behaviors were generated by the selective activation of single command neurons, i.e. that for each unique movement there was a unique command neuron. The ability of single neurons to activate complex outputs involving coor-

© 1988,ElsevierPublications,Cambridge 0378- 5912/88/$0200

TINS, Vol. 1 I, NO. 1 I, 1988