Neural correlates of a default response in a delayed go/no-go task

Abstract

Working memory, the ability to temporarily retain task-relevant information across a delay, is frequently investigated using delayed matching-to-sample (DMTS) or delayed Go/No-Go tasks (DGNG). In DMTS tasks, sample cues instruct the animal which type of response has to be executed at the end of a delay. Typically, performance decreases with increasing delay duration, indicating that working memory fades across a delay. However, no such performance decrease has been found when the sample cues exist of present vs. absent stimuli, suggesting that pigeons do not rely on working memory, but seem to respond by default in those trials. We trained 3 pigeons in a DGNG task and found a similar default response pattern: The diverging slopes of the retention functions on correct Go and No-Go trials suggested that pigeons by default omitted their response following No-Go stimuli, but actively retained task-relevant information across the delay for successful responses on Go trials. We conducted single-cell recordings in the avian nidopallium caudolaterale, a structure comparable to the mammalian prefrontal cortex. On Go trials, many neurons displayed sustained elevated activity during the delay preceding the response, replicating previous findings and suggesting that task-relevant information was neurally represented and maintained across the delay. However, the same units did not show enhanced delay activity preceding correct response suppressions in No-Go trials. This activation-inactivation pattern presumably constitutes a neural correlate of the default response strategy observed in the DGNG task.

Figure 1. Experimental setup and behavioral task.

(A): Stereotaxis and apparatus. The pigeon was placed in front of a screen for stimulus presentation with its head fixed in a stereotaxis for electrophysiological recording. The beak was placed above a small water supplier, and beak movements were controlled with an infrared diode LED attached just above the water reservoir. (B): Sequence of events. Go trials (upper panel) were initiated with the presentation of the Go stimulus. The pigeon had to mandibulate during the response period following a delay of varying duration (0.6 s to 1.4 s). Correct Go responses (hits) were reinforced by access to water; incorrect misses had no consequence. No-Go trials (lower panel) were initiated with the presentation of a No-Go stimulus, followed by a delay. Pigeons had to refrain from responding during the response period. Correct response rejections had no consequences; incorrect false alarms were punished by a brief light-off period.

Figure 2. Behavioral results.

Individual hit and rejection performance for each pigeon, response frequency, and regression lines. (A): Hit performance (% correct) on Go trials as a function of delay duration. (B): Performance in No-Go trials (% correct rejections) as a function of delay duration.

Figure 3. Neuronal activity of a delay neuron recorded over 41 Go trials and 40 No-Go trials.

In the raster plot (top) only Go trials are shown, whereas in the histogram (bottom), spikes are accumulated across all Go (black) and No-Go (grey outline) trials. Vertical lines delineate different time intervals: spontaneous (SP), stimulus (S), delay (Del), response, and control intervals. The beginning of the control interval, which is embedded in the intertrial interval, depends on the animal's behavior and is indicated by a C. In the raster plot, spikes are indicated by short dark lines distributed over the duration of each trial. Open squares indicate responses of the pigeon (i.e., beak openings). Following five positive responses, reinforcement was delivered, indicated by an X. During the delay period, the neuronal activity was elevated in Go trials compared to No-Go trials and other intervals. In addition, the delay activity was increased only in correct Go trials (e.g., Trials 1 through 6), but not after incorrect misses (e.g., Trials 14 through 21).

Figure 4. Neuronal activity of the delay neuron shown in Figure 3 with spikes aligned to the first mandibulation during the response interval (A), the first mandibulation occurring after the control period (B), and to the onset of reward (C).

Figure 5. Activity of 19 delay neurons during different time intervals of the DGNG task (A) and during the delay interval with different delay lengths (B).

The neural activity of each unit was normalized to each unit's spontaneous activity (that equals one) and then to spikes per second, to compensate for the differences in the length of the intervals and the different number of trials for each neuron. A total of 310 hit, 179 miss, 452 correct rejection, and 34 false alarm trials were analyzed.