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      Cortical basis for skilled vocalization

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          We examined the cortical control of a laryngeal muscle that is essential for vocalization in two monkey species that differ in their vocal motor skill. Our results suggest that enhancements in vocal skill are coupled to enlargements in the descending output from two premotor areas, ventral area 6 (area 6V) and the supplementary motor area (SMA). This result challenges the view that improvements in motor skills are due largely to changes in the output from the primary motor cortex.

          Abstract

          Marmosets display remarkable vocal motor abilities. Macaques do not. What is it about the marmoset brain that enables its skill in the vocal domain? We examined the cortical control of a laryngeal muscle that is essential for vocalization in both species. We found that, in both monkeys, multiple premotor areas in the frontal lobe along with the primary motor cortex (M1) are major sources of disynaptic drive to laryngeal motoneurons. Two of the premotor areas, ventral area 6 (area 6V) and the supplementary motor area (SMA), are a substantially larger source of descending output in marmosets. We propose that the enhanced vocal motor skills of marmosets are due, in part, to the expansion of descending output from these premotor areas.

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          Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate.

          Roberta M Kelly, Peter L Strick (2003)
          We used transneuronal transport of neurotropic viruses to examine the topographic organization of circuits linking the cerebellar cortex with the arm area of the primary motor cortex (M1) and with area 46 in dorsolateral prefrontal cortex of monkeys. Retrograde transneuronal transport of the CVS-11 (challenge virus strain 11) strain of rabies virus in cerebello-thalamocortical pathways revealed that the arm area of M1 receives input from Purkinje cells located primarily in lobules IV-VI of the cerebellar cortex. In contrast, transneuronal transport of rabies from area 46 revealed that it receives input from Purkinje cells located primarily in Crus II of the ansiform lobule. Thus, both M1 and area 46 are the targets of output from the cerebellar cortex. However, the output to each area of the cerebral cortex originates from Purkinje cells in different regions of the cerebellar cortex. Anterograde transneuronal transport of the H129 strain of herpes simplex virus type 1 (HSV1) revealed that neurons in the arm area of M1 project via the pons to granule cells primarily in lobules IV-VI, whereas neurons in area 46 project to granule cells primarily in Crus II. Together, the findings from rabies and HSV1 experiments indicate that the regions of the cerebellar cortex that receive input from M1 are the same as those that project to M1. Similarly, the regions of the cerebellar cortex that receive input from area 46 are the same as those that project to area 46. Thus, our observations suggest that multiple closed-loop circuits represent a fundamental architectural feature of cerebrocerebellar interactions.
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            The basal ganglia and the cerebellum: nodes in an integrated network

            Peter L Strick, Andreea Bostan (2018)
            The basal ganglia and the cerebellum are considered to be distinct subcortical systems that perform unique functional operations. The outputs of the basal ganglia and the cerebellum influence many of the same cortical areas but do so by projecting to distinct thalamic nuclei. As a consequence, the two subcortical systems were thought to be independent and to communicate only at the level of the cerebral cortex. Here, we review recent data showing that the basal ganglia and the cerebellum are interconnected at the subcortical level. The subthalamic nucleus in the basal ganglia is the source of a dense disynaptic projection to the cerebellar cortex. Similarly, the dentate nucleus in the cerebellum is the source of a dense disynaptic projection to the striatum. These observations lead to a new functional perspective that the basal ganglia, the cerebellum and the cerebral cortex form an integrated network. This network is topographically organized so that the motor, cognitive and affective territories of each node in the network are interconnected. This perspective explains how synaptic modifications or abnormal activity at one node can have network-wide effects. A future challenge is to define how the unique learning mechanisms at each network node interact to improve performance.
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              Neural pathways underlying vocal control.

              Uwe Jürgens (2002)
              Vocalization is a complex behaviour pattern, consisting of essentially three components: laryngeal activity, respiratory movements and supralaryngeal (articulatory) activity. The motoneurones controlling this behaviour are located in various nuclei in the pons (trigeminal motor nucleus), medulla (facial nucleus, nucl. ambiguus, hypoglossal nucleus) and ventral horn of the spinal cord (cervical, thoracic and lumbar region). Coordination of the different motoneurone pools is carried out by an extensive network comprising the ventrolateral parabrachial area, lateral pontine reticular formation, anterolateral and caudal medullary reticular formation, and the nucl. retroambiguus. This network has a direct access to the phonatory motoneurone pools and receives proprioceptive input from laryngeal, pulmonary and oral mechanoreceptors via the solitary tract nucleus and principal as well as spinal trigeminal nuclei. The motor-coordinating network needs a facilitatory input from the periaqueductal grey of the midbrain and laterally bordering tegmentum in order to be able to produce vocalizations. Voluntary control of vocalization, in contrast to completely innate vocal reactions, such as pain shrieking, needs the intactness of the forebrain. Voluntary control over the initiation and suppression of vocal utterances is carried out by the mediofrontal cortex (including anterior cingulate gyrus and supplementary as well as pre-supplementary motor area). Voluntary control over the acoustic structure of vocalizations is carried out by the motor cortex via pyramidal/corticobulbar as well as extrapyramidal pathways. The most important extrapyramidal pathway seems to be the connection motor cortex-putamen-substantia nigra-parvocellular reticular formation-phonatory motoneurones. The motor cortex depends upon a number of inputs for fulfilling its task. It needs a cerebellar input via the ventrolateral thalamus for allowing a smooth transition between consecutive vocal elements. It needs a proprioceptive input from the phonatory organs via nucl. ventralis posterior medialis thalami, somatosensory cortex and inferior parietal cortex. It needs an input from the ventral premotor and prefrontal cortex, including Broca's area, for motor planning of longer purposeful utterances. And it needs an input from the supplementary and pre-supplementary motor area which give rise to the motor commands executed by the motor cortex.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Proc Natl Acad Sci U S A
                Journal ID (iso-abbrev): Proc Natl Acad Sci U S A
                Journal ID (hwp): pnas
                Journal ID (publisher-id): pnas
                Title: Proceedings of the National Academy of Sciences of the United States of America
                Publisher: National Academy of Sciences
                ISSN (Print): 0027-8424
                ISSN (Electronic): 1091-6490
                Publication date (Electronic): 4 May 2022
                Publication date (Print): 10 May 2022
                Publication date PMC-release: 4 May 2022
                Volume: 119
                Issue: 19
                Electronic Location Identifier: e2122345119
                Affiliations
                [1] aNeurobiology Department, University of Pittsburgh School of Medicine , Pittsburgh, PA 15261;
                [2] bSystems Neuroscience Center, University of Pittsburgh School of Medicine , Pittsburgh, PA 15261;
                [3] cBrain Institute, University of Pittsburgh School of Medicine , Pittsburgh, PA 15261;
                [4] dInstitut de Neurosciences de la Timone CNRS, Aix-Marseille Université , 13005 Marseille, France
                Author notes
                1To whom correspondence may be addressed. Email: strickp@ 123456pitt.edu .

                Contributed by Peter L. Strick; received December 12, 2021; accepted March 23, 2022; reviewed by Asif Ghazanfar and Richard Mooney

                Author contributions: C.M.C., J.-A.R., and P.L.S. designed research; C.M.C. and J.-A.R. performed research; C.M.C., J.-A.R., and P.L.S. analyzed data; and C.M.C., J.-A.R., and P.L.S. wrote the paper.

                Article
                Publisher ID: 202122345
                DOI: 10.1073/pnas.2122345119
                PMC ID: 9171651
                PubMed ID: 35507879
                SO-VID: 15d45dca-5446-416f-b40d-0c04034ee5b4
                Copyright © Copyright © 2022 the Author(s). Published by PNAS.
                License:

                This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).

                History
                Date accepted : 23 March 2022
                Page count
                Pages: 6
                Funding
                Funded by: HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) 100000065
                Award ID: R01NS24328
                Award Recipient : Christina M. Cerkevich Award Recipient : Peter L. Strick
                Funded by: HHS | NIH | National Center for Complementary and Integrative Health (NCCIH) 100008460
                Award ID: R01AT010414
                Award Recipient : Peter L. Strick
                Funded by: HHS | NIH | NIH Office of the Director (OD) 100000052
                Award ID: P40OD010996
                Award Recipient : Peter L. Strick
                Funded by: HHS | NIH | National Institute of Neurological Disorders and Stroke (NINDS) 100000065
                Award ID: T32NS086749
                Award Recipient : Christina M. Cerkevich Award Recipient : Peter L. Strick
                Funded by: DSF Charitable Foundation 100001083
                Award ID: 1805R01
                Award Recipient : Christina M. Cerkevich Award Recipient : Peter L. Strick
                Funded by: DSF Charitable Foundation 100001083
                Award ID: 32RA03
                Award Recipient : Christina M. Cerkevich Award Recipient : Peter L. Strick
                Categories
                Subject: 424
                Subject: Biological Sciences
                Subject: Neuroscience

                Keywords: cerebral cortex,speech,laryngeal muscle,premotor areas
                Data availability:
                Keywords: cerebral cortex, speech, laryngeal muscle, premotor areas

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