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Convergence of forepaw somatosensory and motor cortical projections in the striatum, claustrum, thalamus, and pontine nuclei of cats

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Abstract

The basal ganglia and pontocerebellar systems regulate somesthetic-guided motor behaviors and receive prominent inputs from sensorimotor cortex. In addition, the claustrum and thalamus are forebrain subcortical structures that have connections with somatosensory and motor cortices. Our previous studies in rats have shown that primary and secondary somatosensory cortex (S1 and S2) send overlapping projections to the neostriatum and pontine nuclei, whereas, overlap of primary motor cortex (M1) and S1 was much weaker. In addition, we have shown that M1, but not S1, projects to the claustrum in rats. The goal of the current study was to compare these rodent projection patterns with connections in cats, a mammalian species that evolved in a separate phylogenetic superorder. Three different anterograde tracers were injected into the physiologically identified forepaw representations of M1, S1, and S2 in cats. Labeled fibers terminated throughout the ipsilateral striatum (caudate and putamen), claustrum, thalamus, and pontine nuclei. Digital reconstructions of tracer labeling allowed us to quantify both the normalized distribution of labeling in each subcortical area from each tracer injection, as well as the amount of tracer overlap. Surprisingly, in contrast to our previous findings in rodents, we observed M1 and S1 projections converging prominently in striatum and pons, whereas, S1 and S2 overlap was much weaker. Furthermore, whereas, rat S1 does not project to claustrum, we confirmed dense claustral inputs from S1 in cats. These findings suggest that the basal ganglia, claustrum, and pontocerebellar systems in rat and cat have evolved distinct patterns of sensorimotor cortical convergence.

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Availability of data and material

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Code availability

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Acknowledgements

The authors would like to thank Dr. Michelle Olson and Dr. Kyle Beauchemin for assistance in mounting tissue, as well as Dr. Ron Wilson and the staff at the Penn State Hershey Department of Comparative Medicine for assistance with surgical procedures. This work was supported by NIH grant NS37532 awarded to KDA.

Funding

This work was supported by NIH grant NS37532 awarded to KDA.

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Author notes

  1. Jared B. Smith

    Present address: Target Discovery, REGENXBIO, Inc., Rockville, MD, USA

  2. Shubhodeep Chakrabarti

    Present address: The MathWorks, Stuttgart, Germany

Authors and Affiliations

  1. Department of Neural and Behavioral Sciences, Pennsylvania State University College of Medicine, Hershey, PA, USA

    Jared B. Smith, Shubhodeep Chakrabarti, Todd M. Mowery & Kevin D. Alloway

  2. Center for Neural Engineering, Penn State University, University Park, PA, USA

    Jared B. Smith & Kevin D. Alloway

  3. Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, San Diego, CA, USA

    Jared B. Smith

  4. Rutgers Brain Health Institute, New Brunswick, NJ, USA

    Todd M. Mowery

  5. Department of Otolaryngology, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ, USA

    Todd M. Mowery

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Contributions

Kevin Alloway conceived of the study design. All authors were involved in material preparation. Jared Smith was responsible for data collection, data analysis, making figures and writing the first draft of the manuscript. All authors were involved in editing the manuscript.

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Correspondence to Jared B. Smith.

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The authors declare that they have no conflict of interest. J.B.S. is currently a paid employee of REGENXBIO, Inc. a for-profit company that has no claims or interest in this research. S.C. is currently a paid employee of MathWorks, a for-profit company that has no claims or interest in this research.

Ethical approval

Neuronal tracing experiments were performed on adult felines and all procedures complied with NIH guidelines and were approved by the Penn State Institutional Animal Care and Use Committee (IACUC). Procedures were performed under the guidance of veterinary staff in the Department of Comparative Medicine at the Penn State College of Medicine.

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Smith, J.B., Chakrabarti, S., Mowery, T.M. et al. Convergence of forepaw somatosensory and motor cortical projections in the striatum, claustrum, thalamus, and pontine nuclei of cats. Brain Struct Funct 227, 361–379 (2022). https://doi.org/10.1007/s00429-021-02405-6

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  • DOI: https://doi.org/10.1007/s00429-021-02405-6

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