Behavioral triggers of skin conductance responses and their neural correlates in the primate amygdala

Abstract

The amygdala plays a crucial role in evaluating the emotional significance of stimuli and in transforming the results of this evaluation into appropriate autonomic responses. Lesion and stimulation studies suggest involvement of the amygdala in the generation of the skin conductance response (SCR), which is an indirect measure of autonomic activity that has been associated with both emotion and attention. It is unclear if this involvement marks an emotional reaction to an external stimulus or sympathetic arousal regardless of its origin. We recorded skin conductance in parallel with single-unit activity from the right amygdala of two rhesus monkeys during a rewarded image viewing task and while the monkeys sat alone in a dimly lit room, drifting in and out of sleep. In both experimental conditions, we found similar SCR-related modulation of activity at the single-unit and neural population level. This suggests that the amygdala contributes to the production or modulation of SCRs regardless of the source of sympathetic arousal.

Figures

FIG. 1.

Anatomical reconstruction of recording sites, examples of skin conductance response (SCR)-triggered firing rate averages in 3 single units, and example of SCRs. A: a magnetic resonance imaging (MRI) slice containing the amygdala of monkey T. →, the artifact caused by an array of 7 microelectrodes (80 μm diam each, 600 μm spacing). B: SCR-triggered firing rate averages of 3 single units recorded from the accessory basal nucleus of monkey H during the image viewing task. Traces are in units of SDs from baseline activity (z-score; left axis) and change in firing rate (right axis). The average firing rates of these 3 units from top to bottom were 2.5, 21.3, and 17.3 Hz, respectively. C: typical trace of electrodermal activity with vertical lines marking the onset of skin conductance responses.

FIG. 2.

Probability of SCR occurrence across all sessions as a function of trial progress during the image viewing task. A: in monkey T (▵), the largest number of SCRs occurred during the 3-s image viewing period. Bin size = 200 ms. In monkey H (•), the greatest probability of SCR production occurred just prior to and immediately after image onset. B: skin conductance responses mark the transition between epochs of closed and open eyes within the rest period. Histograms of SCR occurrence in monkeys H and T (top and bottom, respectively) centered on the closing and opening of the eyes. Bin size = 1 s. n = 213 and 225 transitions for monkeys T and H, respectively (all sessions).

FIG. 3.

Neural activity centered on SCR onset in different experimental conditions. Left: panels show the outcome of 3 analyses conducted on the activity of 241 neurons during the image viewing task. Right: panels show the results of the same analyses carried out on 104 neurons recorded during rest. A: summary histograms showing the number of single units with significant (P < 0.01, z test) modulations in firing rate in any of the 250-ms time bins spanning a 20-s window centered on SCR onset (±8 s shown). B: net change in neural activity at the population level surrounding SCR onset. SCR-triggered firing rate averages were calculated for each unit and normalized to their baseline firing rates. At each time point, the population mean (black trace) and median (gray trace) were calculated. The resulting trace (±8 s shown) is expressed in units of SDs away from the mean of the entire 20-s trace (z-score). This convention is carried over into C. The horizontal dotted lines indicate a z-score value of 3. C: absolute change in neural activity at the population level surrounding SCR onset. The traces in C were calculated as in B except that each normalized SCR-triggered average was first converted to changes in the absolute value of the firing rate. The horizontal dotted lines indicate a z-score value of 3. When only response magnitude is considered (A and C), clear SCR-related activity is evident in both experimental conditions. The effects are cancelled out when direction is considered as well (B).

FIG. 4.

Distribution of SCR-related firing rate modulations across the population of single units for both experimental conditions. A: histograms showing the largest change from baseline firing (z-score) observed for each unit during a 2-s period preceding SCR onset. Single units are evenly split between those that show positive and negative changes in firing rate. The magnitudes of these responses are comparable, suggesting 2 distinct populations of units. B: the same histogram as in A but showing only single units recorded from the centromedial nuclei. C: same histogram as in A, but showing only single units recorded from the basolateral nuclei.

FIG. 5.

SCR-related neural activity is not dominated by the opening and closing of the eyes. A–C: depict the results of the same computations as in Fig. 3 with the exclusion of any SCRs occurring within 10 s of the eyes opening or closing during the rest condition. Although this technique had the effect of decreasing the number of highly modulated units (compare A with Fig. 3A), the level of population activity (C) shows the same significant deviation from baseline (z-score >3) as seen in Fig. 3C.