Coding of Object Location in the Vibrissal Thalamocortical System

Cerebral Cortex March 2015;25:563–577 doi:10.1093/cercor/bht241 Advance Access publication September 22, 2013 FEATURE ARTICLE Coding of Object Location in the Vibrissal Thalamocortical System Chunxiu Yu1, Guy Horev2, Naama Rubin, Dori Derdikman, Sebastian Haidarliu and Ehud Ahissar Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel 1Current address: Department of Psychology and Neuroscience, Center for Cognitive Neuroscience, Duke University, Durham, NC 27708, USA 2Current address: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA Address correspondence to E. Ahissar, Department of Neurobiology, Weizmann Institute, Rehovot 76100, Israel. Email: Chunxiu Yu and Guy Horev contributed equally to this work (co-first authors). Keywords: active sensing, anesthetized rats, artificial whisking, convergence dynamics, neuronal representations, touch Introduction Active vibrissal touch is mediated by a hierarchical array of parallel and nested motor-sensory loops (Fig. 1) (Kleinfeld et al. 2006; Bosman et al. 2011). The sensory part of this array conveys information encoded by whisker-object interactions (Szwed et al. 2003; Arabzadeh et al. 2005; Lottem and Azouz 2008; Ritt et al. 2008; Petersen et al. 2009) along at least 4 parallel pathways (Urbain and Deschenes 2007; Diamond et al. 2008). According to data accumulated so far, 2 of these pathways, the paralemniscal and extralemniscal, convey information required for decoding azimuthal object position (Knutsen and Ahissar 2009). The paralemniscal pathway conveys “Whisking” information (information on whisker movement regardless of contacts with external objects) via a rostral sector of the posterior complex of the thalamus (POm) (Sharp and Evans 1982; Yu et al. 2006; de Kock and Sakmann 2009). The extralemniscal pathway conveys “Touch” information (information derived from touch interactions with external objects) via the ventrolateral sector of the ventro-posterior-medial nucleus of the thalamus (VPMvl) (Pierret et al. 2000; Yu et al. 2006). The POm and VPMvl outputs converge in layers 4–6 of the secondary somatosensory cortex (S2) (Carvell and Simons 1987; Alloway et al. 2000; Pierret et al. © The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: 2000), and to a lesser degree in the primary somatosensory cortex (S1) (Pierret et al. 2000). Touch information combined with Whisking information (Whisking/Touch) is also conveyed to S1 by 2 lemniscal pathways (Urbain and Deschenes 2007; Diamond et al. 2008), passing through the “heads’” and “cores’” of VPM barreloids which together form what is termed here the dorso-medial part of VPM (VPMdm) (Yu et al. 2006). Azimuthal object localization by whiskers most likely requires integration of Whisking and Touch signals (Szwed et al. 2003; Curtis and Kleinfeld 2009). Such interactions may occur already at the brainstem level (Furuta et al. 2008). Still, given that separated Whisking and Touch signals exist at the thalamic level (Yu et al. 2006), that rich interactions between pathways (Carvell and Simons 1987; Alloway et al. 2000; Pierret et al. 2000) and signals (Bureau et al. 2006; Crochet and Petersen 2006; Derdikman et al. 2006; Curtis and Kleinfeld 2009; de Kock and Sakmann 2009) occur within the thalamocortical network, that silencing S1 abolishes azimuthal object localization in mice (O’Connor, Clack et al. 2010), and that timed activation of S1 can replace Touch information for azimuthal localization (Venkatraman and Carmena 2011), the working hypothesis of this study was that meaningful internal representations of azimuthal object location are first generated in the thalamocortical network. The vibrissal thalamocortical system is a highly connected and highly interactive network (Hoogland et al. 1987; White and Keller 1987; Agmon and Connors 1992; Deschenes et al. 1994; Bourassa et al. 1995; Gil et al. 1999; Swadlow 2000; Castro-Alamancos and Calcagnotto 2001; Ghazanfar and Nicolelis 2001; Alloway and Roy 2002; Guillery and Sherman 2002; Nicolelis and Fanselow 2002; Alloway et al. 2003; Bruno et al. 2003; Castro-Alamancos 2004; Bokor et al. 2005, 2008; Bruno and Sakmann 2006; Brecht 2007; Groh et al. 2008) embedded within a global motor-sensory closed loop (Fig. 1). In order to eliminate closed-loop effects induced by the global loop, the global loop must be artificially opened. Practically, the motor-sensory loop can be opened in several ways. In one common paradigm the animal is anesthetized and the whiskers are activated passively, thus breaking the muscle-whisker coupling (Fig. 1, “passive”). However, since passive touch activates both Whisking and Touch pathways indiscriminately (Szwed et al. 2003), this approach is not helpful for studying the integration of these 2 types of signals. Thus we employed an alternative approach, in which the animal is anesthetized, the facial motor nerve is cut, and whisking is induced artificially by electrically stimulating the peripheral branch of the motor nerve (Fig. 1, “active”) (Zucker and Welker 1969). With this artificial whisking approach, the mechanics of active In whisking rodents, object location is encoded at the receptor level by a combination of motor and sensory related signals. Recoding of the encoded signals can result in various forms of internal representations. Here, we examined the coding schemes occurring at the first forebrain level that receives inputs necessary for generating such internal representations—the thalamocortical network. Single units were recorded in 8 thalamic and cortical stations in artificially whisking anesthetized rats. Neuronal representations of object location generated across these stations and expressed in response latency and magnitude were classified based on graded and binary coding schemes. Both graded and binary coding schemes occurred across the entire thalamocortical network, with a general tendency of graded-to-binary transformation from thalamus to cortex. Overall, 63% of the neurons of the thalamocortical network coded object position in their firing. Thalamocortical responses exhibited a slow dynamics during which the amount of coded information increased across 4–5 whisking cycles and then stabilized. Taken together, the results indicate that the thalamocortical network contains dynamic mechanisms that can converge over time on multiple coding schemes of object location, schemes which essentially transform temporal coding to rate coding and gradual to labeled-line coding. touch, and thus, also receptor selectivity, can be preserved to a large extent (Zucker and Welker 1969; Szwed et al. 2003; Arabzadeh et al. 2005; Nguyen and Kleinfeld 2005; Derdikman et al. 2006; Yu et al. 2006; Ritt et al. 2008; Lottem and Azouz 2009). Importantly, as this approach involves anesthetized animals, whisking patterns, object contacts and recording sites are fully controlled by the experimenter. Recent fin (...truncated)