A neural correlate of motivational conflict in the superior colliculus of the macaque

Abstract

Behavior is controlled by both external instructions and internal motives, but the actions demanded by each may be different. A common consequence of such a conflict is a delay in decision making and subsequent motor responses. It is unknown, however, what neural mechanisms underlie motivational conflict and associated response delay. To answer this question, we recorded single-neuron activity in the superior colliculus (SC) as macaque monkeys performed a visually guided, asymmetrically rewarded saccade task. A peripheral spot of light at one of two opposing positions was illuminated to indicate a saccade target. In a given block of trials, one position was associated with a big reward and the other with a small reward. The big-reward position was alternated across blocks. Behavioral analyses revealed that small-reward trials created a conflict between the instructed saccade to one position and the internally motivated, yet invalid saccade to the opposite position. We found that movement neurons in the SC temporally exhibited bursting activity after the appearance of the small-reward target opposite their movement field. This transient activity predicted the amount of response delay for upcoming saccades. Our data suggest that motivational conflict activates movement neurons in both colliculi, thereby delaying saccade initiation through intercollicular inhibitory interactions.

FIG. 1.

Visually guided biased saccade task. A: temporal sequences of events. The monkeys first fixated at the central spot of light (“Fixation”). After 1 s the fixation point went off and, simultaneously, the saccade target came on in the periphery (“Target”). The monkeys then made a saccade to the visible target (“Response”). The target was selected pseudorandomly from 2 possible locations, either in the response field of the neuron under study or in the diametrically opposite position. Throughout a block of 20 trials, the saccade to one position was associated with a large reward and the saccade to the other position was associated with a small reward or no reward. B: the 2 kinds of blocks with different position-reward contingencies were alternated while recording from individual neurons.

FIG. 2.

Determination of termination time. A: interspike interval (ISI) histograms for 3 examples of trials from the neuron shown in Fig. 4B. Black circles indicate neuronal spikes; red triangles denote the time of saccade initiation. The termination time (indicated by red arrows) was defined as the time when the ISI exceeded the criterion ISI for the first time after ISI reached the minimum value. The average firing rate during a 40-ms presaccadic period for this neuron was 311 spikes/s when the big-reward target was presented in the response field. Thus the criterion ISI (red solid line) was 42.9 ms with a criterion coefficient of 0.075. For reference, the criterion ISIs with the criterion coefficients of 0.05 and 0.1 are shown by green and orange broken lines, respectively. B: distribution of correlation coefficients between saccadic reaction time (SRT) and termination time. Filled bars indicate neurons with significant positive correlations between SRT and termination time. The means of correlation coefficients with 3 different criterion coefficients were not significantly different from one another (P = 0.79, one-way ANOVA after Fisher's z-transform).

FIG. 3.

Animal performance. A: changes in SRT with changes in the position-reward mapping. The SRT (mean ± 1SD) is plotted as a function of the numerical position of trials in each block for monkey T (top) and monkey S (bottom). Big-reward trials are indicated in blue and small-reward trials in red. Both directions of saccades are combined. B: an example of occasional misdirected saccades observed in small-reward trials (x–y plot of eye position). The monkey first made a saccade in error to the position associated with a big reward (“right-up”) and then changed the saccade direction toward the correct visible target associated with a small reward (“left-down”). FP, fixation point; T, saccade target.

FIG. 4.

An example of paradoxical posttarget activity. A: firing properties of a movement-related neuron recorded in the left superior colliculus (SC). The rastergram is aligned on the onset of the target (time = 0) and shown separately for the target within the response field (right) and away from it (left). Blue backgrounds depict big-reward trials and yellow backgrounds depict small-reward trials. In raster displays, black dots represent individual action potentials and red triangles denote the time of saccade onset. Misdirected saccades are not shown. Top: white dots represent the saccade target; yellow dotted circles represent the response field of this neuron; and gray arrows indicate the animal's saccade. Bottom: the activity during the memory-guided saccade task is shown separately for the saccade made into the response field (right, “RF trials”) and the saccade away from it (left, “nRF trials”); gray triangles denote the time of a GO signal for a saccade (offset of the fixation point); blue continuous lines represent the spike density function. The buildup index was 4.95 for this neuron. B: the raster display for trials in which the small-reward target was presented away from the response field. The trials are sorted according to SRT. The rastergram is aligned on the onset of the target. Red triangles indicate the time of saccade onset. V, vertical eye position; H, horizontal eye position. C: termination time (see methods) is plotted against SRT. One additional trial not shown has the termination time at 0 due to the lack of spikes; see the top trial in B.

FIG. 5.

Another example of paradoxical posttarget activity for a movement-related neuron recorded in the left SC. A–C: same conventions as in Fig. 4. The buildup index was 15.75. Note that the paradoxical posttarget activity of this neuron was preceded by anticipatory pretarget activity.

FIG. 6.

Selective occurrence of the paradoxical posttarget activity. A: the ensemble average activity for movement-related neurons having paradoxical posttarget activity (mean ± SE; n = 41). The activity is aligned on the onset of the target away from the response field and is shown separately for small-reward trials (red) and big-reward trials (blue). The median SRTs for small-reward trials (red arrow) and big-reward trials (blue arrow) are indicated on the horizontal axis. A gray rectangle denotes an epoch during which the neuronal firing rate was quantified in B. B: neuronal firing rate (mean ± 1SD) as a function of trial order from a reversal of the position-reward contingency. Shown are data from the same population of neurons as in A, in which the saccade was made away from the response field. Big-reward trials are indicated in blue and small-reward trials are in red. C: the SRT (mean ± 1SD) as a function of trial order from a reversal of the position-reward contingency. Shown are data from the same sessions as in B (n = 41). Both directions of saccades are combined. Big-reward trials are indicated in blue and small-reward trials in red.

FIG. 7.

Quantitative analyses of the paradoxical posttarget activity. The buildup index is plotted against the correlation coefficient between SRT and termination time. Filled triangles represent neurons with significant positive correlations between SRT and termination time (n = 39). The marginal histograms show the distribution of the correlation coefficient (top) and the buildup index (right). Filled bars indicate neurons with significant positive correlations between SRT and termination time.

FIG. 8.

Comparison of neuronal activity between the sampled neuron (“orthoneuron”) and its theoretical counterpart (“antineutron”) for big-reward trials (A–C) and small-reward trials (D–F).

FIG. 9.

Effects of motivational conflict on neuronal activity. A: the ensemble average activity on big-reward trials (left) and small-reward trials (right) for all of the movement-related neurons studied (n = 62). The activity is aligned on the onset of the target and drawn until the median SRT. c-SC, SC contralateral to the target; i-SC, SC ipsilateral to the target. B: a schematic illustration of presumed behavioral processes influencing the intercollicular inhibitory interactions. The command for the saccade to the visual target is issued from c-SC. Presumed inhibitory interneurons are omitted.