Research reportSensory cortical dynamics
Introduction
Although understanding of the neural basis of perception is far from complete, it is clear that the computations that underlie perception are carried out quickly, a necessity if the challenges posed by an ever-changing environment are to be met successfully. For instance, Thorpe et al. [47] demonstrated that humans can make sensory decisionsādetermining whether or not a complex scene contains a particular elementāin less than 200 ms. Given the rapidity of this decision, it seems likely that cells involved in processing the information needed for this task rely primarily on rapid synaptic neurotransmission (e.g. AMPA and NMDA receptor mediated excitatory neurotransmission, and GABAA receptor mediated inhibitory transmission). Traditionally, fast neural computation is viewed as occurring in essentially stable or āhard-wiredā networks; that is, networks whose processing characteristics are independent of their recent history of activation. On a much longer time scale (e.g. days or years), it has been established that cortical networks can undergo substantial changes in functional connectivity in response to prolonged alterations in the pattern of sensory drive (i.e. experience-based cortical plasticity, [5]). These long-term changes in functional connectivity are believed to involve changes in synaptic efficacy and/or axonal sprouting.
These two views of the information processing characteristics of primary sensory cortexāa fixed circuit capable of rapid processing, and a plastic network capable of long-term changeāare conventionally regarded as distinct features of cortical networks. The two extremes, however, may not be as dichotomous as is commonly believed. Rather, we propose that they form opposing ends of a continuum of functional states that can be expressed by primary sensory cortex, each state having information processing capacities maximally consistent with the properties of the stimuli the network processed in a preceding temporal interval. Central to this alternative view is the idea that a stimulus applied either continuously or intermittently at a sufficient rate evokes an orderly temporal continuum of functional states in primary sensory cortex. We refer to the hypothesized temporal progression of functional network states associated with temporally extended sensory stimulation as ācortical dynamicsā. The available experimental evidence leads us to believe that natural sensory stimulation evokes cortical dynamics which (1) occur over a time scale of tens of milliseconds to many minutes; (2) are associated with an orderly temporal progression of changes in the receptive field properties of primary sensory cortical neurons; and (3) involve a repertoire of linked cellular mechanisms, each requiring unique conditions for its activation, and each exhibiting a distinct time course of operation.
In this brief review, we present evidence obtained using both single neuron and neuronal population recording methods which supports our concept of sensory cortical dynamics. We also introduce a substantial literature describing cellular mechanisms with attributes compatible with short-term, reversible, use-dependent changes in sensory cortical networks. We conclude with a discussion of the potential functional benefits of cortical network dynamics.
Section snippets
Single neuron dynamics
Contrary to the view that the response properties of primary sensory cortical neurons are fixed in the short term, there is considerable experimental evidence that the selectivity and response characteristics of sensory cortical neurons evolve continuously during the presentation of a stimulus. For example, the selectivity of individual sensory cortical neurons has been shown to change dramatically and rapidly (in tens of milliseconds) after stimulus onset. Sugase et al. [45] reported that the
Population dynamics
While evidence concerning stimulus-driven dynamics in single sensory cortical neurons has been accruing for decades, detailed information about the temporal evolution of the neuronal population response to persistent or repetitive sensory stimulation has become available only within the past few years. In general, these studies have shown that the changes in response observed at the single-cell level are paralleled by substantial and orderly dynamics occurring at the level of the responding
Mechanisms of dynamics
That the response properties of sensory cortical neurons undergo substantial transient stimulus-driven change is not surprising given a rich substrate of potential cellular and synaptic mechanisms which could contribute to these dynamics. For instance, the response of a neuron to even the most basic stimulusāthe injection of depolarizing current into the somaādepends on its recent activity. Due to the presence of calcium-activated potassium channels, the firing rate of pyramidal cells during
Benefits of sensory cortical dynamics
The available experimental evidence suggests that by affecting the response properties of cortical neurons, stimulus-driven dynamics alter substantially the information processing characteristics of cortical networks. There are several, interrelated functional benefits which may be provided by cortical network dynamics. In essence, all of the suggested benefits propose that stimulus-drive causes a rapid and stimulus-specific optimization of the network. First, although fewer cortical neurons
Conclusion
Stimulus-evoked sensory drive transiently alters the response properties of individual sensory cortical neurons and modifies the size of the responding neuronal population. The alterations that accompany temporally extended sensory stimulation are fully consistent with the biophysical characteristics of the somal and dendritic compartments of cortical neurons and the properties of cortical synaptic neurotransmission. Sensory cortical dynamics may result in the significant enhancement of the
Acknowledgements
This work was supported by NIH RO1 NS34979 and NS37501 (BW) and an NIMH predoctoral NRSA (AK). We thank Wyeth Bair and Matt Smith for helpful comments.
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