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A Multisensory Perspective Onto Primate Pulvinar Functions Mathilda Froesel, Céline Cappe, Suliann Ben Hamed

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A Multisensory Perspective Onto Primate Pulvinar Functions Mathilda Froesel, Céline Cappe, Suliann Ben Hamed A multisensory perspective onto primate pulvinar functions Mathilda Froesel, Céline Cappe, Suliann Ben Hamed To cite this version: Mathilda Froesel, Céline Cappe, Suliann Ben Hamed. A multisensory perspective onto primate pulv- inar functions. Neuroscience & Biobehavioral Reviews, Oxford: Elsevier Ltd., 2021, 125, pp.231-243. 10.1016/j.neubiorev.2021.02.043. hal-03219659 HAL Id: hal-03219659 https://hal.archives-ouvertes.fr/hal-03219659 Submitted on 6 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Neuroscience and Biobehavioral Reviews 125 (2021) 231–243 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev A multisensory perspective onto primate pulvinar functions Mathilda Froesel a,*, C´eline Cappe b, Suliann Ben Hamed a,* a Institut des Sciences Cognitives Marc Jeannerod, CNRS UMR 5229, Universit´e Claude Bernard Lyon I, 67 Boulevard Pinel, 69675, Bron Cedex, France b Centre de Recherche Cerveau et Cognition, Universit´e Paul Sabatier, Universit´e de Toulouse, 31062, Toulouse Cedex 9, France ARTICLE INFO ABSTRACT Keywords: Perception in ambiguous environments relies on the combination of sensory information from various sources. Pulvinar Most associative and primary sensory cortical areas are involved in this multisensory active integration process. Cortex As a result, the entire cortex appears as heavily multisensory. In this review, we focus on the contribution of the Multisensory pulvinar to multisensory integration. This subcortical thalamic nucleus plays a central role in visual detection Visual and selection at a fast time scale, as well as in the regulation of visual processes, at a much slower time scale. Auditory Somatosensory However, the pulvinar is also densely connected to cortical areas involved in multisensory integration. In spite of Anatomy this, little is known about its multisensory properties and its contribution to multisensory perception. Here, we fMRI review the anatomical and functional organization of multisensory input to the pulvinar. We describe how visual, auditory, somatosensory, pain, proprioceptive and olfactory projections are differentially organized across the main subdivisions of the pulvinar and we show that topography is central to the organization of this complex nucleus. We propose that the pulvinar combines multiple sources of sensory information to enhance fast re­ sponses to the environment, while also playing the role of a general regulation hub for adaptive and flexible cognition. 1. Introduction Though the activity of these sensory areas are dominated by one sensory modality, there is now ample evidence that they are modulated Vision is the dominant sensory modality in both humans and by other sensory modalities, including at the earliest processing levels nonhuman primates. Up to 50 % of identified non-human primate (Brosch et al., 2005; Calvert et al., 1999; Cl´ery et al., 2015a; Foxe et al., functional areas are involved in visual processing (20–30 % in the 2000; Ghazanfar et al., 2005; Giard and Peronnet, 1999; Guipponi et al., humans, (Van Essen and Drury, 1997; Van Essen, 2003)). As a result, 2015; Kayser et al., 2008; von Kriegstein et al., 2005; Lakatos et al., vision is still to date the most studied sensory system. This contrasts with 2007; Molholm et al., 2002). For example, neuronal activity in the pri­ the rising view that perception and brain functions are intrinsically mary visual cortex is modulated by auditory (Wang et al., 2008) as well multisensory (Schroeder and Foxe, 2005). For example, audition, touch as by tactile stimulations (Guipponi et al., 2015). At the anatomical and proprioception play a crucial role in the sensory-motor exploration level, direct projections between early sensory areas have been of the world. Likewise, audition, olfaction and touch are essential to described, between the somatosensory and visual cortex (Cappe et al., social interactions and communication. These different sensory modal­ 2012, 2009a; Cappe and Barone, 2005). At higher cortical levels, in the ities have very similar anatomical organizational principles in the brain: associative cortices, multisensory convergence and integration is the incoming sensory information from the distal sensory receptors are rule (Noesselt et al., 2007; Werner and Noppeney, 2010; Calvert, 2001; transduced into a neuronal code and reach the cortex through special­ Bremmer et al., 2001; Miller and D’Esposito, 2005; Avillac et al., 2007; ized primary sensory cortical areas (Fig. 1, colored cortex, Van Essen Guipponi et al., 2013), to the degree that the entire brain is often et al., 1990; Carmichael et al., 1994; Camalier et al., 2012). From there, considered as of multisensory nature (Cl´ery et al., 2018a, 2015a; Clery´ this sensory information runs through a sequence of reciprocally con­ and Ben Hamed, 2018; Driver and Noesselt, 2008; Ghazanfar and nected cortical regions, organized along a hierarchical pattern, pro­ Schroeder, 2006; Schroeder and Foxe, 2005). Most of these associative gressively describing the incoming sensory information at higher levels multisensory areas have direct projections to and from early sensory of complexity (Fig. 1, associative cortices). areas. For example, superior temporal polysensory area (STP), activated * Corresponding authors. E-mail addresses: [email protected] (M. Froesel), [email protected] (S. Ben Hamed). https://doi.org/10.1016/j.neubiorev.2021.02.043 Received 6 March 2020; Received in revised form 18 February 2021; Accepted 25 February 2021 Available online 1 March 2021 0149-7634/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). M. Froesel et al. Neuroscience and Biobehavioral Reviews 125 (2021) 231–243 projections (Rouiller and Welker, 2000; Sherman, 2007). Based on these highly complex cortico-pulvino-cortical connectivity patterns, the pulvinar is proposed to play a key role as a mediator/modulator between cortical areas (Benarroch, 2015; Saalmann and Kastner, 2011). In the following, we specifically focus onto the primate pulvinar, which is classically divided in three large distinct regions, based on their specific cytoarchitectonic properties: the lateral, the medial and the inferior pulvinar (Fig. 2, Walker, 1938; Olszewski, 1952; Gutierrez et al., 1995; Stepniewska and Kaas, 1997). The organization of the primate pulvinar complex and its connectivity with the cortex has undergone substantial changes during primate evolution (Kaas and Baldwin, 2020). Specifically,while the visual inferior and ventro-lateral pulvinar nuclei are well preserved across primates, the medial pulvinar is considered as fully identifiableonly in the haplorhini primate suborder (Baldwin et al., 2017; Homman-Ludiye and Bourne, 2019), but not in the non-haplorhini primates such as the galagos or the lemurs. The rodent and carnivore Fig. 1. Organization of main sensory input to the primate brain,visual in homologues of the pulvinar can be defined based on the observed pink, somatosensory in purple and auditory in green. These cortices are pattern of projections of the superficial layers of the superior colliculus dominated by responses to one sensory modality and are reciprocally connected or optic tectum to the primate pulvinar (Zhou et al., 2017). In spite of the to the rest of the cortex in so called-associative areas, i.e. areas associating or integrating together multiple sensory inputs. fact that pulvinar lesions in these latter mammalian phylogenetic orders do not exhibit the same visual deficitsas in primates, a certain functional and cortical connectivity pattern homology can be noted between the by both auditory and somatosensory information, has direct projections lateral-posterior pulvinar complex of rodents and carnivores and the to primary visual area V1 (Clavagnier et al., 2004). In addition, they are primate inferior and ventro-lateral pulvinar nuclei (Kaas and Baldwin, characterized by specific laminar and connectional patterns with 2020). No homologue for the medial primate pulvinar can be identified cortical and subcortical structures (Foxworthy et al., 2013). in rodents and carnivores as is the case for non-haplorhini primates (Kaas Overall, multisensory integration thus involves complex patterns of and Baldwin, 2020). multisensory interactions i) within associative areas, ii) between distant While the contribution of the pulvinar to visual cognition has been associative areas, iii) between associative areas and early sensory extensively studied including during development (Benarroch, 2015; cortices, iv) within early sensory cortices and v) between distant early Bourne and Morrone, 2017; Bridge et al., 2016), we will here focus onto sensory cortices. All sensory information reaches the neocortex through its contribution to multisensory processes and its interactions with the the thalamus and the superior colliculus. In turn, both these subcortical
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