Ascending vestibular pathways to parietal areas MIP and LIPv and efference copy inputs from the medial reticular formation: Functional frameworks for body representations updating and online movement guidance

Abstract

The posterior parietal cortex (PPC) serves as a sensorimotor interface by integrating multisensory signals with motor related information for generating and updating body representations and movement plans. Using retrograde transneuronal transfer of rabies virus combined with a conventional tracer, we identified direct and polysynaptic pathways to two PPC areas, the rostral medial intraparietal area (MIP) and the ventral part of the lateral intraparietal area (LIPv) in macaque monkeys. We found that rostral MIP and LIPv receive ascending vestibular pathways, and putative efference copy inputs disynaptically from the medullary medial reticular formation (MRF) where reticulospinal pathways to neck and arm motoneurons originate. LIPv receives minor disynaptic vestibular inputs, and substantial projections from the head movement‐related rostral MRF, consistent with head gain modulation of LIPv activity and a role in planning gaze shifts. Rostral MIP is the target of prominent disynaptic pathways from reaching‐ and head movement‐related MRF domains, and major ascending vestibular pathways trisynaptically from both labyrinths, explaining prominent vestibular responses and discrimination between active and passive movements demonstrated in rostral MIP and in the neighboring ventral intraparietal area, which are heavily interconnected. The findings that rostral MIP (belonging to the ‘parietal reach region’), receives vestibular inputs as directly as classical vestibular areas, via a parallel channel, and efference copy signals pathways from MRF reticulospinal domains that belong to reach and head movement networks have important implications for the understanding of the role of the PPC in updating body representations and internal models for online guidance of movement.

Pathways from the superior colliculus and the nucleus of the optic tract to the posterior parietal cortex in macaque monkeys: Functional frameworks for representation updating and online movement guidance

“…The experiments were carried out at the appropriate biosafety containment level. Details on preparation of rabies virus, handling of animals and the methodology for transneuronal tracing using rabies virus were described in detail previously (Prevosto et al, 2009(Prevosto et al, , 2010(Prevosto et al, , 2011Ugolini, 1995Ugolini, , 2010Ugolini, , 2011Ugolini, , 2020Ugolini et al, 2006Ugolini et al, , 2019.…”

“…Injections were made at the end of long-term electrophysiological recordings (MIP and LIPv: MSTl: Ilg & Schumann, 2007) and targeted at stereotaxic coordinates of previously recorded responses. Neuronal properties in rostral MIP and LIPv were described earlier (see Ugolini et al, 2019). The injections into MSTl were targeted at the site of previously recorded smooth pursuit-related activity with extra-retinal components (Ilg et al, 2004;Ilg & Schumann, 2007).…”

“…The injection needle was left in place for more than 30 min after the end of the injection. After recovery from general anaesthesia, the animals acted normally without any clinical or behavioural signs of infection for the entire duration of the study (Prevosto et al, 2009(Prevosto et al, , 2010(Prevosto et al, , 2011Ugolini et al, 2019).…”

“…We have studied the origin of direct and polysynaptic inputs to PPC areas in macaque monkeys, that is, the rostral medial intraparietal area (MIP), the ventral part of the lateral intraparietal area (LIPv) and the lateral subdivision of the middle superior temporal area (MSTl), using retrograde transneuronal transfer of rabies virus combined with a conventional tracer (Figures 1 and 2) (Prevosto et al, 2009(Prevosto et al, , 2010(Prevosto et al, , 2011Ugolini, 1995Ugolini, , 2010Ugolini, , 2011Ugolini, , 2020Ugolini et al, 2019). Clarifying the origin of inputs to these cortical areas is critical for understanding the mechanisms supporting their operations.…”

“…Zones of fibrosis due to multiple recording traces are seen in the white matter ventral to LIPv (e, h) or dorsomedial to the MIP injection site (f, i). (LIPv and MIP images are modified with permission from Ugolini et al, 2019Ugolini et al, , 50: 2988 The SC is a crucial node for mediating sensorimotor transformations for action. It integrates different sensory modalities with motor and cognitive inputs from multiple cortical areas and the cerebellum (May, 2006;Wurtz & Albano, 1980).…”