Interspike Intervals, Receptive Fields, and Information Encoding in Primary Visual Cortex

Daniel S. Reich, Ferenc Mechler, Keith P. Purpura, Jonathan D. Victor
2000 Journal of Neuroscience  
In the primate primary visual cortex (V1), the significance of individual action potentials has been difficult to determine, particularly in light of the considerable trial-to-trial variability of responses to visual stimuli. We show here that the information conveyed by an action potential depends on the duration of the immediately preceding interspike interval (ISI). The interspike intervals can be grouped into several different classes on the basis of reproducible features in the interspike
more » ... nterval histograms. Spikes in different classes bear different relationships to the visual stimulus, both qualitatively (in terms of the average stimulus preceding each spike) and quantitatively (in terms of the amount of information encoded per spike and per second). Spikes preceded by very short intervals (3 msec or less) convey information most efficiently and contribute disproportionately to the overall receptive-field properties of the neuron. Overall, V1 neurons can transmit between 5 and 30 bits of information per second in response to rapidly varying, pseudorandom stimuli, with an efficiency of ϳ25%. Although some (but not all) of our results would be expected from neurons that use a firing-rate code to transmit information, the evidence suggests that visual neurons are well equipped to decode stimulus-related information on the basis of relative spike timing and ISI duration. Cortical sensory neurons have high intrinsic temporal precision (Mainen and Sejnowski, 1995; Nowak et al., 1997) and can encode information on the scales of milliseconds and tens of milliseconds (Buračas and Albright, 1999) . Three questions arise immediately. (1) What kinds of stimuli are encoded on the different time scales in a neuron's response? (2) How much information is encoded on each time scale? (3) How might this information be decoded by relatively simple components of neurons and neural circuits? Here, we answer the first two questions experimentally by measuring the responses of neurons in the primary visual cortex (V1) of macaque monkeys to rapidly varying, pseudorandom ("m-sequence") stimuli. The interspike intervals (ISIs) of spike trains fired by these neurons fall into three subsets, distinguished on the basis of ISI duration, in a stereotyped manner across neurons. We use a reverse-correlation procedure to generate receptive field (RF) maps from the full responses as well as from response subsets that only contain spikes that follow ISIs of particular durations. Finally, we use information theory to quantify the rate and efficiency with which full responses and response subsets convey messages about the visual stimulus. Our results indicate that spikes in different ISI subsets are fired in response to different visual stimuli. In particular, spikes preceded by ISIs Ͻ3 msec, which occur during periods of very high firing rate, tend to be evoked by stimuli that have several subregions of opposite contrast covering the neuron's receptive field. Each of these spikes also tends to convey more stimulus-related information than the average spike. On the other hand, spikes preceded by ISIs Ͼ38 msec are often fired in response to spatially uniform stimuli that reverse contrast over time. The third question, concerning the ways in which these different messages are decoded, is not addressed directly by our experiments. We note at the outset that this question is conceptually independent from another much-debated question in cortical physiology: whether cortical neurons encode information through a rate code or a temporal code. In fact, both types of code can generate receptive-field maps and information rates similar to what is described here. However, the existence of stereotyped ISI durations in V1 (described in this paper), together with recently described synaptic and dendritic machinery (such as depression, facilitation, and coincidence detection) that can selectively increase or decrease the importance of particular spikes in shaping a postsynaptic response, suggests that real-time decoding of neuronal signals may rely on known biophysical mechanisms specifically sensitive to ISI duration. MATERIALS AND METHODS Recording and stimuli. We recorded the responses of single V1 neurons in opiate-anesthetized macaque monkeys . All experimental procedures complied with the guidelines of the National Eye Institute and our institution. We measured spike times to the nearest 0.1 msec for 135 neurons, and to the nearest 3.7 msec (one frame of the visual display) for 36 neurons. We include in our analysis only the 99 neurons [32 simple, 60 complex, and 7 unclassified (Skottun et al., 1991)] that responded with firing rates higher than 3 spikes/sec and that had significantly modulated RF maps (see below). Our stimuli look to human observers like random and rapidly flickering checkerboards. In fact, however, the stimuli are highly structured. They consist of a grid in which the temporal sequence of the luminance levels (0 or 300 cd /m 2 ) in each of 249 pixels (typically 16 ϫ 16 arc-min) is determined by a pseudorandom, binary m-sequence (Sutter, 1992; Victor, 1992; Reid et al., 1997) . The same 4095 step m-sequence is used in each pixel, but the starting position in the sequence is different. Because
doi:10.1523/jneurosci.20-05-01964.2000 pmid:10684897 fatcat:rb6aby7lafhq3opst3kyx3xvg4