Corticothalamic feedback and sensory processing

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Abstract

Although nearly half of the synaptic input to neurons in the dorsal thalamus comes from the cerebral cortex, the role of corticothalamic projections in sensory processing remains elusive. Although sensory afferents certainly establish the basic receptive field properties of thalamic neurons, increasing evidence indicates that feedback from the cortex plays a crucial role in shaping thalamic responses. Here, we review recent work on the corticothalamic pathways associated with the visual, auditory, and somatosensory systems. Collectively, these studies demonstrate that sensory responses of thalamic neurons result from dynamic interactions between feedforward and feedback pathways.

Introduction

The cerebral cortex receives almost all of its sensory input from the thalamus. With the exception of olfaction, sensory information is delivered to cortical neurons through excitatory connections made by thalamic cells known as relay neurons. Although the name relay neuron might suggest that these cells simply pass the baton of sensory activity from the periphery to the cortex, it has become increasingly clear that these neurons are members of a complex circuit that involves ascending, descending, and recurrent sets of neuronal connections (Figure 1; 1., 2., 3.).

The major source of descending input to thalamic relay neurons comes from neurons with cell bodies located in layer 6 of the cerebral cortex (Figure 1). These corticothalamic neurons exert both an excitatory and an inhibitory influence on relay neurons, and it is the balance of this excitation and inhibition that is thought to influence many of the activity patterns and sensory response properties of relay neurons (reviewed in 4., 5., 6.). The excitatory influence of the cortex is achieved by monosynaptic connections that are markedly robust in number. Indeed, the number of corticothalamic synapses made onto a relay neuron is much greater than the number of synapses made from any other single source, including the ascending pathways from the periphery 7., 8., 9.. The inhibitory influence of the cortex, on the other hand, is achieved by polysynaptic connections either with intrinsic γ-amino butyric acid (GABA)ergic interneurons within the relay nuclei or with GABAergic neurons with cell bodies located in the reticular nucleus (RTN) of the thalamus 1., 2., 3..

Given the number of inputs provided to thalamic relay cells by corticothalamic neurons, it has been tempting to speculate what functional role these corticothalamic pathways could serve. Despite the certain importance of the corticothalamic pathway for thalamic processing, a consensus about its function has been elusive. Proposed roles for cortical feedback fall into two general categories: first, to effect sensory responses and receptive field properties, and second, to effect firing mode and/or activity state. Several excellent reviews discussing this second category of proposed roles have recently been published 4., 5., 6., 10., 11., 12., 13., 14., 15., 16.. In this review, we focus our discussion on the first category — the effects of cortical feedback on sensory responses and receptive field properties. As the anatomical properties of cortical feedback are so similar for the visual, auditory, and somatosensory systems, it seems reasonable to suggest that the role(s) of feedback should generalize across systems. By identifying the effects of corticothalamic input that are shared by multiple sensory systems, we hope to present results that will foster a consensus in thinking about corticothalamic function. Thus, our approach will be to identify and describe effects of feedback that are shared by more than one sensory system. In particular, we focus our discussion of the role of corticothalamic feedback for visual, auditory, and somatosensory processing by examining results from studies of sensory responses in the lateral geniculate nucleus (LGN), medial geniculate body (MGB), and ventrobasal complex (VB).

Section snippets

Corticothalamic feedback, receptive fields and sensory filtering

Before describing the influence of cortical feedback on sensory responses in the thalamus, it is important to review briefly the receptive field properties of thalamic neurons (Figure 2). In general, neurons in the LGN, MGB, and VB have receptive fields that can be described in terms of a discrete region in sensory space in which appropriate stimuli evoke an excitatory response. In addition to this excitatory region, neurons in all three thalamic nuclei often display a larger and more subtle

Corticothalamic feedback and egocentric selection

In addition to sharpening thalamic receptive fields by increasing the effectiveness of center (excitatory) and surround (suppressive) mechanisms, corticothalamic feedback could also play a role in what has been termed ‘egocentric selection’. Egocentric selection refers to the ability of cortical neurons to analyze thalamic input, determine which sensory features are encoded in the thalamic response, and then amplify the transmission of these selected features by feedback to the thalamus. This

Conclusions and future directions

It has become increasingly clear that thalamic neurons are not mere relays of sensory activity, but, rather, components of an elaborate circuit designed to perform complex computations for sensory processing. By comparing results from the visual, auditory, and somatosensory systems, corticothalamic feedback has been found to function in both the sharpening of thalamic receptive fields and the packaging of sensory information most suited for cortical processing.

Future studies that are aimed at

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

We thank M Sutter and K McAllister for comments on previous versions of this manuscript. WM Usrey is supported by National Institutes of Health grants EY13588, EY12576, the McKnight Foundation, the Esther A and Joseph Klingenstein Fund, and the Alfred P.Sloan Foundation.

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