Anatomical pathways that link perception and action

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Abstract

Pathways linking action to perception are generally presented as passing from sensory pathways, through the thalamus, and then to a putative hierarchy of corticocortical links to motor outputs or to memory. Evidence for more direct sensorimotor links is now presented to show that cerebral cortex rarely, if ever, receives messages representing receptor activity only; thalamic inputs to cortex also carry copies of current motor instructions.

Pathways afferent to the thalamus represent the primary input to neocortex. Generally they are made up of branching axons that send one branch to the thalamus and another to output centers of the brain stem or spinal cord. The information transmitted through the classical “sensory” pathways to the thalamus represents not only information about the environment and the body, but also about instructions currently on their way to motor centers.

The proposed hierarchy of direct corticocortical connections of the sensory pathways is not the only possible hierarchy of cortical connections. There is also a hierarchy of the corticofugal pathways to motor centers in the midbrain, and there are transthalamic corticocortical pathways that may show a comparable hierarchy. The extent to which these hierarchies may match each other, and relate to early developmental changes are poorly defined at present, but are important for understanding mechanisms that can link action and perception in the developing brain.

Introduction

The functional relationship between action and perception has in the past been viewed in two distinct ways. The first looks for the functional links that lead from a sensory event, through several stages of subcortical and cortical perceptual processing to a motor action that is appropriate to that sensory event, or to a record in memory for later action (Fig. 1). This approach can relate neural actions and neural pathways to particular behavioral situations and provide information about the nerve cells that are involved at each stage in the sensory–motor interaction. Examples include neural recordings made at early stages of sensory processing (Mountcastle et al., 1963; Talbot et al., 1968; Hubel and Wiesel, 1977; Vallbo et al. 1979), but from the point of view of this workshop are most tellingly illustrated by records of neural activity obtained from higher cortical areas in awake animals (Gallant et al., 1998; Cook and Maunsell, 2002Tsao et al., 2003). In such studies, the relevant cortical areas are generally assumed to lie on a hierarchical chain of corticocortical pathways that leads from the primary receiving areas of cortex to higher areas concerned eventually with memory or motor outputs (Felleman and Van Essen, 1991). This view is based on an initial assumption about the afferent pathways, amply confirmed experimentally (Adrian, 1928; Kuffler, 1953; Perl et al., 1962; Barlow, 2004), that the messages carried to the brain from the eye, the ear, the muscle receptors, the skin etc. function to inform the central sensory pathways about events impinging on peripheral receptors. That is, that they represent external events. Churchland et al. (1994), writing critically about such a view of vision, have referred to it as a “theory of pure vision”, and one can generalize and think of it as a theory of pure sensation. In this chapter, I argue that such a view, while clearly in accord with known relationships between sensory events and neural activity in ascending pathways to cortex, ignores the fact that the neural activity reaching cortex represents more than merely the information about events that impinge on peripheral receptors. This review shows that it also represents a pattern of instructions that are already on their way to lower motor centers before any of the messages can reach cortex (see Fig. 2and Section 2; Guillery and Sherman, 2002a; Guillery, 2003).

An alternative view of the relationship between action and perception can be obtained by considering illusory perceptions, misperceptions, or failed perceptions that can lead to inappropriate actions or interpretations (Gibson, 1933; Festinger et al., 1967; Churchland et al., 1994; O’Regan and Noe¨, 2001). The observations are generally based on subtle experimental approaches to puzzling and often elusive perceptual phenomena or motor actions. These observations serve to illustrate conclusions that perception is much more closely related to activity in the motor pathways (the “sensorimotor contingencies” of O’Regan and Noe¨, 2001) than generally recognized by the first view. This second approach, including, for example, that of Helmholtz (see translation by Warren and Warren, 1968) or of Sperry (1952) has, in one way or another, played an important role in accounts that see action as an essential part of perception. However, in general, wherever one looks at evidence of this sort, relating action to perception, the physical links, that is, the anatomical pathways involved, are poorly defined or undefined, except near the periphery (see the motor link from ascending afferents to motor centers in Fig. 2), and these peripheral links are almost invariably ignored by contemporary studies of sensory processing.

Churchland et al. (1994) are exceptional in providing a summary of some of the anatomical pathways that might play a role in this second approach to action and perception. Having considered the many back projections that go from cortex not only to the thalamus but also to motor centers such as the superior colliculus and the striatum, they conclude that “the anatomy is consistent with the idea that motor assembly can begin even before sensory signals reach the highest levels”. The pathways summarized in Fig. 2and mentioned above, show not only that motor assembly can begin before the sensory signals reach the highest levels but that the motor and sensory signals are inextricably bound to each other on their way to the thalamus; the motor assembly must begin before sensory signals reach the highest levels. This review presents evidence that afferents to the thalamus are commonly made up of branching axons that send one branch to the thalamus for transfer to cortex and another branch to motor or premotor1 centers for a role in action. That is, these branching axons, which carry the messages to the thalamus for transfer to cortex, are sending to cortex something more than the information about activity in peripheral receptors. They are also providing the cortex with information about the instructions that have already been sent to the motor centers. Currently very little is known about the nature of most of these motor instructions. They may be for preparation, facilitation, or inhibition of movement. The crucial point is that these motor instructions form an essential part of the messages that reach the first stages of cortical perceptual processing. Even though they can be separated in the mind of the neuroscientist who is studying the sensory pathways, they can never be separated by the cortical area in receipt of the messages. Again, very little is known about the functions of these motor collaterals in relation to sensory functions, because they have not been studied from this point of view in the past.

In addition to the motor links shown in Fig. 2, evidence is presented that there are also transthalamic corticocortical pathways (Fig. 3), which provide potentially equally important links between action and perception. As shown in this figure, the message that is passed from one cortical area through the thalamic relay to another cortical area, is commonly (perhaps always) also transmitted by a branch of the corticothalamic axon to a motor or premotor center (Guillery and Sherman, 2002a; Guillery, 2003). These branching axons show that some of the pathways that link one cortical area to another are, like the ascending pathways to cortex, involved in two intimately related functions that need to be distinguished if one wishes to understand cortical processing. One is to forward messages from one cortical area, through the thalamus, to another cortical area, and the other is to inform one cortical area about the outputs that the other (lower) cortical area is sending to motor or premotor centers of the brain.

Section snippets

“Driver” pathways to the thalamus and their motor branches

There is a basic pattern of organization that is common to the whole of the thalamus, which has been considered in more detail in several earlier publications (Guillery, 1995; Sherman and Guillery, 1996, Sherman and Guillery, 2001, Sherman and Guillery, 2002; Guillery and Sherman, 2002a, Guillery and Sherman, 2002b; Sherman, 2005). In summary, all thalamic relays receive a small proportion of afferents that resemble, in their structure and synaptic relationships, the sensory “drivers”

Descending axons from cortical layer 5

One issue often overlooked when cortical functions in perceptual processing are being considered is that most, probably all, cortical areas have major outputs from cells in layer 5 to lower brainstem centers (Fig. 4). The roles of these cortical areas in corticocortical perceptual processing will necessarily be closely linked to their other roles, which are more closely related to the motor control systems innervated in the brainstem. It is relevant to recall that the surprise generated by

The anatomy of sensorimotor contingencies and its development

If one looks at the brainstem premotor and motor connections of incoming ascending (sensory) afferents to thalamus schematized in Fig. 2, one can see that they establish connections that are likely to contribute to a motor action unless other, higher pathways counteract this action. These connections can be regarded as a first step in the production of the sensorimotor motor contingencies that are basic to our perceptual performance. Helmholtz (Warren and Warren, 1968), considering how

The hierarchies of cortical functions and pathways

The cortical areas concerned with vision have been described as forming a rough hierarchy on the basis of the direct corticocortical connections (Felleman and Van Essen, 1991), and it is possible that a comparable rough hierarchy will be identifiable on the basis of relationships established by the transthalamic corticocortical pathways. Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8, Fig. 9, Fig. 10 raise several important questions in highly simplified form: (1) Do the patterns of connections

Conclusions

This study has considered pathways that demonstrate close ties between sensory processing on the one hand and involvement in motor instructions on the other. These are ties provided by branching axons, indicating that for most pathways afferent to the thalamus, and thus for most inputs to the cerebral cortex, the two functions are inextricably linked. As shown in Fig. 12, most messages relayed through the thalamus, possibly all of them, bring information of these two sorts to the cortex. The

Acknowledgments

The author thanks Murray Sherman, Keith Kluender, and Art Glenberg for comments on an earlier draft and Sherry Feig for Fig. 9, Fig. 10.

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