Single unit activity in marmoset posterior parietal cortex in a gap saccade task

Abstract

Abnormal saccadic eye movements can serve as biomarkers for patients with several neuropsychiatric disorders. To investigate cortical control mechanisms of saccadic responses, the common marmoset (Callithrix jacchus) is a promising non-human primate model. Their lissencephalic brain allows for accurate targeting of homologues of sulcal areas in the macaque brain. Here we recorded single unit activity in the posterior parietal cortex of two marmosets using chronic microelectrode arrays, while the monkeys performed a saccadic task with Gap trials (stimulus onset lagged fixation point offset by 200ms) interleaved with Step trials (fixation point disappeared when the peripheral stimulus appeared). Both marmosets showed a gap effect-shorter saccadic reaction times (SRTs) in Gap vs.Step trials. On average, stronger gapperiod response across the entire neuronal population preceded shorter SRTs on trials with contralateral targets, although this correlation was stronger among the 15% 'gap neurons', which responded significantly during the gap. We also found 39% 'target neurons' with significant visual target-related responses, which were stronger in Gap trials and correlated with the SRTs better than the remaining cells. Compared with slow saccades, fast saccades were preceded by both stronger gap-related and target-related response in all PPC neurons, regardless of whether such response reached significance. Our findings suggest that the PPC in the marmoset contains an area that is involved in the modulation of saccadic preparation and plays roles comparable to those of area LIP in macaque monkeys in eye movements. SIGNIFICANCE STATEMENTAbnormal saccadic eye movements can serve as biomarkers for different neuropsychiatric disorders. So far, processes of cerebral cortical control of saccades are not fully understood. Non-human primates are ideal models for studying such processes, and the marmoset is especially advantageous since their smooth cortex permits laminar analyses of cortical microcircuits. Using electrode arrays implanted in the posterior parietal cortex of marmosets, we found neurons responsive to key periods of a saccadic task in a manner that contribute to cortical modulation of saccadic preparation. Notably, this signal was correlated with subsequent saccadic reaction times and was present in the entire neuronal population. We suggest that the marmoset model will shed new light on the cortical mechanisms of saccadic control.

Interspecies activation correlations reveal functional correspondences between marmoset and human brain areas

“…On the other hand, the area surrounding the marmoset IPS have also been linked to the attention-like frontoparietal network by several RS-fMRI studies (Ghahremani et al, 2016; Hori et al, 2020b). It is also known that electrical microstimulation in the areas surrounding the IPS evoke saccadic eye movements (Ghahremani et al, 2019) and that single neurons in the region show neural correlates for the gap effect in saccadic eye movement tasks (Ma et al, 2020). As such, it seems that parietal areas surrounding the IPS in the marmoset are involved in both default mode and attention networks.…”

“…The common marmoset has become an important nonhuman primate model for bridging the translational gap between rodents and humans. Marmosets have a lissencephalic cortex, like rodents, but as primates they possess the structural and functional brain architecture that supports elaborated behaviors such as pro-social interaction (Ferrari and Digby, 1996; Huang et al, 2020; Miller et al, 2016; Saito, 2015; Yokoyama and Onoe, 2015), complex vocal communication (Choi et al, 2015; Miller et al, 2015; Sadagopan et al, 2015; Takahashi et al, 2016), and saccadic eye movements (Chen et al, 2020; Ma et al, 2020; Mitchell et al, 2014; Selvanayagam et al, 2019). This, paired with a high reproductive power, small size, and fast maturation rate, make this non-human primate (NHP) species particularly interesting for neuroscience.…”

Marmosets: a promising model for probing the neural mechanisms underlying complex visual networks such as the frontal–parietal network

“…Electrophysiological recordings in macaque area LIP have also revealed that most neurons discharge in the 'planning stage', just prior to the execution of saccades towards visible and remembered visual targets (Gnadt and Andersen 1988;Barash et al 1991;Colby et al 1996;Meister et al 2013) within their response fields. For example, during saccade tasks where the end target onset is delayed after the fixation target disappears, a "gap effect" of shorter saccade reaction times coupled with an increase in neural activity during the gap period has been recorded in macaques (Chen et al 2013(Chen et al , 2016 as well as marmosets (Ma et al 2020). Generally, area LIP neurons respond to a combination of visual stimuli, eye position and the direction and amplitude of planned eye movements, to encode the location of salient visual stimuli in eye-centered or headcentred coordinates (Andersen et al 1985(Andersen et al , 1990b.…”

“…Express saccades, or saccades with very low latencies, can be elicited using a 'gap' saccade task, in which the central fixation point disappears prior to the saccade target onset. Humans, macaques, and marmosets all exhibit low-latency express saccades in a gap-saccade task (Ma et al 2020;Chen et al 2021). Marmosets can also perform smooth pursuit eye movements, in which the eye voluntarily tracks a moving target, with similar velocity and acceleration profiles to macaques and humans .…”

“…To date, marmoset studies have yet to demonstrate delayed responses to visual stimuli. Fixation durations have been shorter (approximately 1 second, for example in (Ma et al 2020)). The shorter fixation duration makes delayed-saccade tasks more challenging.…”