The sensorimotor slice

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Abstract

The reciprocal connections between primary motor cortex (M1) and primary somatosensory cortex (S1) are hypothesized to play a role in an animal's ability to update its motor plan in response to changes in the sensory periphery. These interactions provide the sensory cortex with anticipatory knowledge of motor plans. In the mouse neocortex there are representations of the body surface within both M1 and S1. Utilizing physiologically targeted micro injections of biotinylated dextran amine into either the whisker representation of M1 (wM1) or S1 (wS1) we characterized the axonal pathways connecting these two areas. We then used this data to determine a plane of section that contained both whisker M1 and whisker S1 and maintained the axonal pathway between these two areas. In vitro physiological studies demonstrated that excitatory synaptic connections are maintained in this novel plane of section. The sensorimotor slice is an ideal preparation to study inter-areal cortical connectivity.

Introduction

Both sensory and motor cortices contain finely scaled topographic maps (Woolsey, 1952; Brooks et al., 1961, Li and Waters, 1991). These maps allow both primary motor cortex (M1) and primary somatosensory cortex (S1) to have highly specialized responses to changes in the periphery, allowing for precise execution of motor tasks. S1 and M1 are reciprocally connected yet the functional influence of these interactions remains unknown. In primates, S1 inactivation can result in disruption of chewing (Lin et al., 1993, 1998; Hiraba et al., 2000), fine motor coordination, sustained muscle contraction, appropriate grip force and the ability to determine the weight of an object (Rothwell et al., 1982, Johansson and Westling, 1984, Hikosaka et al., 1985; Brochier et al., 1999). These results suggest that motor control can strongly be influenced by S1 inputs. Understanding the pathway between S1 and M1 is an important first step towards comprehending how sensorimotor computations are preformed.

Despite the role that intercortical connections have in cognitive computations, research has traditionally focused on the response properties (in vivo studies) or the physiological properties (in vitro studies) of neurons found in specific cortical areas. Furthermore, little research has focused on interactions between cortical areas, especially those serving different functions (e.g. sensory and motor). The lack of a model preparation that contains interconnected cortical areas has been a hindrance to this line of research and the development of such a preparation is an important step towards understanding intercortical connectivity.

At present, it is unknown what pathways the axons that connect S1 and M1 traverse, or what their synaptic targets are. In the case of the rodent somatosensory, visual and auditory systems it is possible to cut a slice that contains both the thalamus and cortex with some degree of connectivity maintained (Agmon and Connors, 1991, Cruikshank et al., 2002, MacLean et al., 2006). Despite the fact that motor cortex and somatosensory cortex are adjacent to each other little work has been done to develop a slice which contains these two areas and their reciprocal connections. The advantage of a slice that contains S1 and M1 would be the ability to study the relationship between cortical feedforward and feedback networks in the same slice. A similar approach has been utilized to effectively study the interactions and the spread of epileptic activity between the hippocampus and adjacent cortical areas such as the entorhinal cortex (Breustedt et al., 2002) or the parahippocampal cortex (Bear and Lothman, 1993). In order to study the interconnectivity between whisker M1 and whisker S1 we have developed an in vitro preparation that contains the whisker representations of M1 and S1 and maintains their synaptic interconnectivity.

Section snippets

Materials and methods

All experiments were performed on white laboratory adult Swiss mice (CD-1, postnatal day 30–60) of either sex (Charles River Laboratories, Wilmington, MA). All experiments were performed in accordance with the Institutional Animal Care and Use Committee guidelines of Queens College, CUNY.

Results

We created an in vitro preparation that contains the whisker representations of both primary motor and primary sensory areas while also maintaining their synaptic interconnectivity. The precise locations of wM1 and wS1 were identified via microstimulation and electrophysiological methods, respectively. In our anatomical studies, both areas of interest were marked and the brain was subsequently hemisected and sectioned at a 45° angle relative to the midline. We found this angle of sectioning to

Discussion

The results of the present study indicate that it is possible to create a slicing plane such that the primary motor and primary somatosensory areas are contained within one slice. Furthermore, we demonstrate that the reciprocal synaptic connectivity between these two areas is maintained within this novel plane of section. The sensorimotor slice preparation will be a useful tool for studying sensorimotor integration in specific and inter-areal cortical communication in general.

Acknowledgements

Thanks to the laboratory for helpful discussions and encouragement. Annamaria Barczak and Aileen Tlamsa for experimental assistance. Thanks to Jonathan Levitt and Raddy Ramos for helpful discussions and comments on the manuscript. The work was supported by PSC-CUNY (6006-33-35) and CUNY-Collaborative Grants to J.C.B.

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