Ongoing activity in the optic tectum is correlated on a trial-by-trial basis with the pupil dilation response

Abstract

Netser S, Dutta A, Gutfreund Y. Ongoing activity in the optic tectum is correlated on a trial-by-trial basis with the pupil dilation response. J Neurophysiol 111: 918 -929, 2014. First published December 4, 2013; doi:10.1152/jn.00527.2013.-The selection of the appropriate stimulus to induce an orienting response is a basic task thought to be partly achieved by tectal circuitry. Here we addressed the relationship between neural activity in the optic tectum (OT) and orienting behavioral responses. We recorded multiunit activity in the intermediate/deep layers of the OT of the barn owl simultaneously with pupil dilation responses (PDR, a well-known orienting response common to birds and mammals). A trial-by-trial analysis of the responses revealed that the PDR generally did not correlate with the evoked neural responses but significantly correlated with the rate of ongoing neural activity measured shortly before the stimulus. Following this finding, we characterized ongoing activity in the OT and showed that in the intermediate/ deep layers it tended to fluctuate spontaneously. It is characterized by short periods of high ongoing activity during which the probability of a PDR to an auditory stimulus inside the receptive field is increased. These high-ongoing activity periods were correlated with increase in the power of gamma band local field potential oscillations. Through dual recordings, we showed that the correlation coefficients of ongoing activity decreased as a function of distance between recording sites in the tectal map. Significant correlations were also found between recording sites in the OT and the forebrain entopallium. Our results suggest that an increase of ongoing activity in the OT reflects an internal state during which coupling between sensory stimulation and behavioral responses increases.

Noise correlations in the owl optic tectum are differentially impacted by unimodal vs crossmodal competitors

“…NCs evoked by auditory or visual stimulation were measured for 182 and 181 neuronal pairs, respectively. Values ranged from -0.30 to 0.80 (auditory) and -0.22 to 0.93 (visual), a range consistent with a previous report of 14 spontaneously active pairs in owl OT (Netser, Dutta, and Gutfreund 2014). Overall, the mean noise correlation evoked by auditory or visual stimulation was 0.28 and 0.25, respectively.…”

“…Evoked NC values ranged from -0.35 to 0.94, with a mean of 0.28, 0.25, and 0.28 for auditory, visual, and bimodal, respectively. These values are consistent with a prior report of 14 OTd pairs recorded in response to spontaneous activity (Netser, Dutta, and Gutfreund 2014). A recent study using tetrodes in OTd and auditory stimulation reported somewhat lower values, with mean NC values of 0.13 (Beckert, Pavao, and Pena 2017).…”

Overt Responses during Covert Orienting

“…Thus, multisensory processing in the SCi (Stein and Meredith, 1993) may also mediate the pupil responses evoked by salient stimuli. Finally, while the robustness of the link between the SCi and salience-evoked pupil dilation remains to be established with recording studies in the monkey, very recent evidence in the owl links aspects of activity in the optic tectum with pupil dilation responses (Netser et al, 2014). Thus, like the neck and shoulder, the SCi has the necessary projections and response properties to modulate salient pupil responses, independent of the OPNs.…”

Physiological phenotyping of dementias using emotional sounds

“…Here we took nonverbal sound as a model system to investigate systematically the physiological and behavioral correlates of processing sensory emotional salience in patients with canonical dementia syndromes. We used pupillometry to index autonomic (sympathetic) reactivity: compared with other candidate autonomic indices [36] , [37] , [38] , pupil dilatation responses are relatively resistant to disease-associated movement and other artifacts, well preserved to auditory stimuli in healthy older individuals [39] , track neural responses closely [23] , [40] , [41] , and have social behavioral resonance [42] , [43] . We used affective valence ratings to index the behavioral processing of auditory emotional salience.…”