Time as coding space?
Introduction
In investigations of neuronal correlates of behaviour, the measured neuronal variable is typically the stimulus- or action-related modulation of the discharge rate of neurons. This approach has led to an impressive body of evidence relating variations in the discharge rate of individual neurons to specific cognitive and motor processes. However, unless these variations of discharge rate are tightly time-locked to stimuli or motor events, this approach precludes assessment of information that could, in principle, be encoded in the precise temporal relations between the discharges of ensembles of neurons that contribute collectively to a particular function. Such information can be extracted only from multi-cell recordings and correlation analysis of simultaneously registered neuronal responses.
A steadily increasing number of studies has focused on the temporal properties of neuronal responses (reviewed in 1, 2, 3). These follow the discovery of precise synchronisation of neuronal responses in the visual cortex induced by stimuli but resulting from internal interactions and therefore not time-locked to the temporal structure of the inducing stimulus. It is undisputed that behaviourally relevant information is encoded in graded and event-related rate fluctuations of neuronal responses (e.g. the rate-coded population vectors in the motor cortex [4]). However, it is currently a matter of controversy whether neurons in the central nervous system can distinguish with sufficient temporal precision between synchronised and temporally dispersed synaptic input in order to exploit precise temporal relations among converging synaptic activity for the encoding of information. Studies pertinent to this issue have been performed at many different levels; for example, electrophysiological analysis of synaptic integration in ex vivo preparations, single- and multi-cell recordings in vivo in a variety of species (ranging from insects to primates), noninvasive examinations of electrical activity in human brains, psychophysical analysis of temporal integration in human subjects and computer simulations. I review here experiments that have examined temporal features of neuronal integration at different levels of analysis.
Section snippets
Transmission of temporal stimulus features
Behavioural analyses and electrophysiological recording have long shown that the neuronal networks involved in binaural sound localisation can resolve time delays between the inputs from the two ears in the submillisecond range, implying extremely precise transmission of temporal stimulus features and hence very short time constants for synaptic integration [5]. Evidence that other systems, including neocortical circuits, are also capable of handling temporal information with a precision in the
Cellular signals
If neuronal networks can operate with high temporal precision and if precisely synchronised synaptic inputs are more effective than temporally dispersed EPSPs, precise temporal relations among the discharges of distributed neurons can, in principle, be exploited for coding. First, synchronisation could be used for response selection because it enhances the saliency of discharges with great temporal selectivity. Second, by virtue of the fact that saliency increases simultaneously and selectively
Synchrony and learning
If precise timing relations among the discharges of distributed neurons are used not only to convey information about the temporal structure of stimuli but also as a mechanism for the selection and grouping of responses, learning mechanisms must operate with similar temporal resolution. Recent evidence indicates that use-dependent modifications of synaptic gain such as long-term potentiation (LTP) and long-term depression (LTD) are indeed dependent on very precise temporal relations between
Synchronisation as a signature of relatedness
The results reviewed so far provide correlative evidence for a role of response synchronisation in neuronal processing but permit no stringent inferences as to whether the nervous system attributes significance to the precise temporal relations among discharges. Recent psychophysical studies in humans, however, have exploited the fact that responses of neurons in the visual cortex can be made synchronous by synchronising the stimuli that evoke them, with a precision similar to that reached by
Conclusions
The studies reviewed here allow us to draw four main conclusions about neuronal networks. First, they can handle temporal information with high precision. Second, they transmit synchronised activity with more efficiency than asynchronous activity. Third, through internal interactions, they can generate precise temporal relations among distributed discharges that are independent of the temporal structure of stimuli. Finally, they interpret the synchronisation of discharges as signature of
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
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