A causal role for pulvinar in coordinating task independent cortico-cortical interactions

Abstract

planned and conceptualized the study. M. K. E and M. A. P performed the experiments. M. K. E and M. A. P performed analysis. M. K. E. and S. K. prepared the draft. M. K. E, M. A. P and S. K. reviewed and edited the final draft. AbstractPulvinar is the largest nucleus in the primate thalamus and has topographically organized connections with multiple cortical areas, thereby forming extensive cortico-pulvino-cortical input-output loops. Neurophysiological studies have provided evidence for a role of these transthalamic pathways in regulating information transmission between cortical areas. However, a causal role of pulvinar in regulating cortico-cortical interactions has not yet been demonstrated. In particular, it is not known whether pulvinar's influences on cortical networks are taskdependent or reflect more basic large-scale network properties that maintain functional connectivity across a network regardless of active task demands. In the current study, under a passive viewing condition, we conducted simultaneous electrophysiological recordings from interconnected ventral (area V4) and dorsal (LIP) nodes of the macaque visual system while reversibly inactivating the dorsal part of lateral pulvinar (dPL), which shares common anatomical connectivity with V4 and LIP. Our goal was to probe a causal role of pulvinar in regulating cortico-cortical interactions in the absence of any active task demands. Our results show a significant reduction in local field potential phase coherence between LIP and V4 in low frequencies (4-15 Hz) following muscimol -a potent GABAA agonist -injection into dPL. At the local level, no significant changes in firing rates or LFP power were observed in LIP or in V4 following dPL inactivation. These results indicate a causal role for pulvinar in synchronizing neural activity between interconnected cortical nodes of a large-scale network, even in the absence of an active task state. Significance StatementPulvinar, the largest nucleus of the primate thalamus, has been implicated in several cognitive functions. The extensive cortico-pulvino-cortical loops formed by pulvinar are suggested to be regulating information transmission between interconnected cortical areas. However, a causal evidence for pulvinar's role in cortico-cortical interactions in the absence of active task demands is not yet clear. We conducted simultaneous recordings from nodes of macaque visual system (areas V4 and LIP) while inactivating the dorsal part of the lateral pulvinar (dPL) under a passive viewing condition. Our results show a significant reduction in local field phase coherence between LIP and V4 in low frequencies ( 4-15 Hz) following inactivation of dPL, thus providing evidence for a causal role of pulvinar in regulating cortico-cortical interactions even in the absence of an active task state.

The Missing Link in Early Emotional Processing

“…Two reasons have been mentioned suggesting that the pulvinar is probably not the core IES. On one hand, the main inputs to visual pulvinar are descending projections from different visual cortices, which shapes its main role as a hub that coordinates cortico-cortical activity (Eradath et al, 2020;Jaramillo et al, 2019). On the other hand, reported latencies of pulvinar enhanced activity towards emotional stimulation seem, up to the present, longer than required to explain initial visual cortex responses to emotional stimuli, as reviewed above.…”

“…Innervations are mutual: these PI subdivisions send projections to the same visual areas from which they receive inputs. Thus, the pulvinar is mainly considered as a cortico-cortical intercommunication and coordination hub (Eradath et al, 2020;Jaramillo et al, 2019).…”

The Missing Link in Early Emotional Processing

“…Two evidences have been mentioned suggesting that the pulvinar is probably not the core of the IESs network. First, the main inputs to visual pulvinar are descending projections from different visual cortices, and its main role is acting as a hub that coordinates cortico-cortical activity (Eradath et al, 2020;Jaramillo et al, 2019). Second, reported latencies of pulvinar enhanced activity towards emotional stimulation seem, up to the present, longer than required to explain initial visual cortex responses to emotional stimuli, as reviewed above.…”

“…Innervations are mutual: these PI subdivisions send projections to the same visual areas from which they receive inputs. Thus, the pulvinar is mainly considered as a cortico-cortical intercommunication and coordination hub (Eradath et al, 2020;Jaramillo et al, 2019). Particularly, this role as a cortical hub could consist in regulating "cortico-cortical information flow by modifying synaptic efficacy within and across visual cortical regions, rather than by relaying visual features from one area to another" (Halassa & Kastner, 2017, p. 1673.…”

The Missing Link in Early Emotional Processing

“…Innervations are mutual: these PI subdivisions send projections to the same visual areas from which they receive inputs. Thus, the pulvinar is mainly considered a cortico-cortical intercommunication and coordination hub (Eradath et al, 2020; Jaramillo et al, 2019). Particularly, this role as a cortical hub could consist in regulating “cortico-cortical information flow by modifying synaptic efficacy within and across visual cortical regions, rather than by relaying visual features from one area to another” (Halassa & Kastner, 2017, p. 1673).…”