Spatiotemporal activity patterns of rat cortical neurons predict responses in a conditioned task

Abstract

Precise and repeated spike-train timings within and across neurons define spatiotemporal patterns of activity. Although the existence of these patterns in the brain is well established in several species, there has been no direct evidence of their influence on behavioral output. To address this question, up to 15 neurons were recorded simultaneously in the auditory cortex of freely moving rats while animals waited for acoustic cues in a Go/NoGo task. A total of 235 significant patterns were detected during this interval from an analysis of 13 hr of recording involving over 1 million spikes. Of particular interest were 129 (55%) patterns that were significantly associated with the type of response the animal made later, independent of whether the response was that prompted by the cue because the response occurred later and the cue was chosen randomly. Of these behavior-predicting patterns, half (59/129) were associated with an enhanced tendency to go in response to the stimulus, and for 11 patterns of this subset, trials including the pattern were followed by significantly faster reaction time than those lacking the pattern. The remaining behavior-predicting patterns were associated with an enhanced NoGo tendency. Overall mean discharge rates did not vary across trials. Hence, these data demonstrate that particular spatiotemporal patterns predict future behavioral responses. Such presignal activity could form templates for extracting specific sensory information, motor programs prespecifying preference for a particular act, and/or some intermediate, associative brain process.

Figure 1

(A) An example of a pattern formed by activity in two cells recorded from two different electrodes in the same hemisphere. Details of pattern timing are shown at Left. In the Center, several action potential waveforms from each cell are overlaid (scale bars for cell # 11 apply to both). Vertical lines on the traces are superimposed markers relating to settings of the template-matching software used to discriminate the waveforms. Right, all detected examples of the pattern formed by these cells displayed in rasters. Each tick mark shows the occurrence of an action potential, and each row shows a segment of data in which a pattern was detected. The rows have been slid past one another such that the first spikes of each occurrence of the pattern are aligned (a spike of cell # 5 at time 0). The accurate timing between that spike and a subsequent spike in cell # 11 and a later spike of cell # 5 causes these later spikes to also line up in the display, forming the nearly vertical lines at 320 ± 3 and 662 ± 3 ms delay. In this example, the data shown includes trials recorded on two consecutive days, as detailed in B. (B) Relationship of occurrence of pattern shown in A to Go-vs.-NoGo task performance. The possible behavioral situations in which Go and NoGo responses could occur are illustrated schematically (Upper). Go responses resulted both from correct movements to the feeder in response to low-pitch sound at the right speaker (*L) and from incorrect movements when a high pitch was delivered to this speaker (H). Conversely, NoGo responses could be correct (high pitch to right speaker) or incorrect (failure to move in response to low pitch to right speaker). Lower shows dot rasters of the same data shown in A but on a compressed time scale and aligned to the time of stimulus onset instead of to time of the first spike of the pattern. The trials are divided into those in which Go (Left) and NoGo (Right) responses occurred. Spikes involved in generating instances of the pattern during the waiting period (time to the left of the stimulus onset) are displayed as bars instead of ticks. Three spikes constituting one instance of the pattern are denoted by open circles. Note that there are more than twice as many Go trials (n = 27) with patterns than NoGo trials (n = 12), although the total number of Go and NoGo responses was nearly the same (n = 283 and 269, respectively). In addition, in this example the reaction time for Go responses with a pattern (825 ± 60 ms) was significantly shorter than for Go responses with no pattern (985 ± 23 ms).

Figure 2

An example of a NoGo pattern formed by activity in two cells recorded from the same electrode. Details of pattern timing are shown at Upper Left. Upper Right shows the behavioral conditions corresponding to the NoGo behavior (see Fig. 1). (Lower) Each small tick mark shows the occurrence of an action potential, and each row shows a segment of data in which a pattern was detected. The rows have been slid past one another such that the first spikes of each occurrence of the pattern are aligned (a spike of cell # 4). The accurate timing between that spike and a subsequent spike in cell # 3 and a later spike of cell # 4 causes these later spikes to also line up in the display, forming the nearly vertical lines at 25 ± 4 and 406 ± 2 ms delay with respect to pattern onset. Note that this pattern repeated 19 times but occurred only during the NoGo trials. In this session, the rat performed 29 Go trials and 90 NoGo trials.