Optical imaging reveals functional domains in primate sensorimotor cortex

Abstract

Motor cortex (M1) and somatosensory cortex (S1) are central to arm and hand control. Efforts to understand encoding in M1 and S1 have focused on temporal relationships between neural activity and movement features. However, it remains unclear how the neural activity is spatially organized within M1 and S1. Optical imaging methods are well-suited for revealing the spatio-temporal organization of cortical activity, but their application is sparse in monkey sensorimotor cortex. Here, we investigate the effectiveness of intrinsic signal optical imaging (ISOI) for measuring cortical activity that supports arm and hand control in a macaque monkey. ISOI revealed spatial domains that were active in M1 and S1 in response to instructed reaching and grasping. The lateral M1 domains overlapped the hand representation and contained a population of neurons with peak firing during grasping. In contrast, the medial M1 domain overlapped the arm representation and a population of neurons with peak firing during reaching. The S1 domain overlapped the hand representations of areas 1 and 2 and a population of neurons with peak firing upon hand contact with the target. Our single unit recordings indicate that ISOI domains report the locations of spatial clusters of functionally related neurons. ISOI is therefore an effective tool for surveilling the neocortex for “hot zones” of activity that supports movement. Combining the strengths of ISOI with other imaging modalities (e.g., fMRI, 2-photon) and with electrophysiological methods can open new frontiers in understanding the spatio-temporal organization of cortical signals involved in movement control.

Neural activity is spatially clustered in motor and dorsal premotor cortex

“…Pixel darkening peaked several seconds after movement onset. Our time courses from single sessions were consistent with those reported in the few studies that used ISOI with forelimb tasks (Friedman et al, 2020a;Heider et al, 2010). Our three control experiments confirmed that the relatively slow negative peaks were predicated on movement execution.…”

“…The necessary implementation here is to image entire forelimb representations during arm and hand actions then quantify the spatial organization of movement-related cortical activity. Intrinsic signal optical imaging (ISOI), 2-photon imaging, and fMRI have been successfully used in measuring cortical activity related to arm and hand actions in monkeys (Ebina et al, 2018; Friedman et al, 2020a; Kondo et al, 2018; Nelissen and Vanduffel, 2011). The mesoscopic field-of-view in ISOI is particularly well-suited for the size of the forelimb representations in M1 and PMd.…”

Continuous long‐term recording and triggering of brain neurovascular activity and behaviour in freely moving rodents

“…An alternative strategy is the measurement of reflected light from brain tissue (optical intrinsic signal or OIS). This method has been used for decades as a technique for measuring brain neurovascular activity (Kim et al 2017;Kura et al 2018;Friedman et al 2020). OIS comprises multiple components, including blood, cell volume/extracellular space, and intracellular organelles such as mitochondria (Chang et al 2010;Pan et al 2018;Woo et al 2019;Friedman et al 2020).…”

“…This method has been used for decades as a technique for measuring brain neurovascular activity (Kim et al 2017;Kura et al 2018;Friedman et al 2020). OIS comprises multiple components, including blood, cell volume/extracellular space, and intracellular organelles such as mitochondria (Chang et al 2010;Pan et al 2018;Woo et al 2019;Friedman et al 2020). The relative contribution of these components varies with the wavelength of light that is reflected.…”

Exploring EEG spectral and temporal dynamics underlying a hand grasp movement

“…It was demonstrated [ 50 ] that grasp-related neural activity was observed in the ventral premotor F5, parietal AIP, the cortical F1 areas pertaining to the hand field and in the several regions of the somatosensory cortex. An intrinsic spatial optical imaging (ISOI) study [ 51 ] had explored spatial domains that were active in M1 and S1 in response to reaching and grasping in macaque monkeys.…”