Long-Range Neuronal Circuits Underlying the Interaction between Sensory and Motor Cortex

Janelia Farm Research Campus, HHMI, 19700 Helix Drive, Ashburn, VA 20147, USA.
Neuron (Impact Factor: 15.05). 10/2011; 72(1):111-23. DOI: 10.1016/j.neuron.2011.07.029
Source: PubMed


In the rodent vibrissal system, active sensation and sensorimotor integration are mediated in part by connections between barrel cortex and vibrissal motor cortex. Little is known about how these structures interact at the level of neurons. We used Channelrhodopsin-2 (ChR2) expression, combined with anterograde and retrograde labeling, to map connections between barrel cortex and pyramidal neurons in mouse motor cortex. Barrel cortex axons preferentially targeted upper layer (L2/3, L5A) neurons in motor cortex; input to neurons projecting back to barrel cortex was particularly strong. Barrel cortex input to deeper layers (L5B, L6) of motor cortex, including neurons projecting to the brainstem, was weak, despite pronounced geometric overlap of dendrites with axons from barrel cortex. Neurons in different layers received barrel cortex input within stereotyped dendritic domains. The cortico-cortical neurons in superficial layers of motor cortex thus couple motor and sensory signals and might mediate sensorimotor integration and motor learning.

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Available from: Tianyi Mao, Nov 20, 2014
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    • "In addition, the cortical areas can form the connections for their respective innate signals to be associated and for one of them to be able to encode the associated signals. The barrel cortex meets these requirements since it is located at the dorsal surface of the cerebral cortex (Shepherd and Svoboda, 2005; Aronoff et al., 2010; Mao et al., 2011) and connects with the piriform cortex in cross-modal plasticity (Ye et al., 2012). The barrel cortex encodes whisker tactile sensation (Petersen, 2007) and the piriform cortex receives odor signal (Barkai and Saar, 2001; Wilson, 2001; Wilson and Sullivan, 2012). "
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    ABSTRACT: Associative learning and memory are essential to logical thinking and cognition. How the neurons are recruited as associative memory cells to encode multiple input signals for their associated storage and distinguishable retrieval remains unclear. We studied this issue in the barrel cortex by in vivo two-photon calcium imaging, electrophysiology, and neural tracing in our mouse model that the simultaneous whisker and olfaction stimulations led to odorant-induced whisker motion. After this cross-modal reflex arose, the barrel and piriform cortices connected. More than 40% of barrel cortical neurons became to encode odor signal alongside whisker signal. Some of these neurons expressed distinct activity patterns in response to acquired odor signal and innate whisker signal, and others encoded similar pattern in response to these signals. In the meantime, certain barrel cortical astrocytes encoded odorant and whisker signals. After associative learning, the neurons and astrocytes in the sensory cortices are able to store the newly learnt signal (cross-modal memory) besides the innate signal (native-modal memory). Such associative memory cells distinguish the differences of these signals by programming different codes and signify the historical associations of these signals by similar codes in information retrievals.
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    • "In order to sensibly interact with the world and skilfully manipulate objects, information needs to be shared between the somatosensory and motor systems (Rossi et al., 1998; Brochier et al., 1999; Nelson et al., 2004). The two systems communicate via a network of extensive connections between the sensory and motor cortices (Asanuma et al., 1968; Strick & Preston, 1978; Stepniewska et al., 1993; Andersson, 1995; Huffman & Krubitzer, 2001; Makris et al., 2005; Shinoura et al., 2005; Eickhoff et al., 2010; Mao et al., 2011; Catani et al., 2012), but also by motor cortex cells responding directly to sensory stimuli (Albe-Fessard & Liebeskind, 1966; Goldring & Ratcheson, 1972; Fetz et al., 1980; Fromm et al., 1984) and sensory cortex cells controlling motor behaviour (Matyas et al., 2010). Despite having relatively good knowledge of the anatomical substrate for communication between the primary sensory and motor cortices, particularly with respect to the hand (Hikosaka et al., 1985), our understanding of what information is transferred remains poor. "
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    ABSTRACT: Moving and interacting with the world requires that the sensory and motor systems share information, but while some information about tactile events is preserved during sensorimotor transfer the spatial specificity of this information is unknown. Afferent inhibition (AI) studies, in which corticospinal excitability (CSE) is inhibited when a single tactile stimulus is presented before a transcranial magnetic stimulation pulse over the motor cortex, offer contradictory results regarding the sensory-to-motor transfer of spatial information. Here, we combined the techniques of AI and tactile repetition suppression (the decreased neurophysiological response following double stimulation of the same vs. different fingers) to investigate whether topographic information is preserved in the sensory-to-motor transfer in humans. We developed a double AI paradigm to examine both spatial (same vs. different finger) and temporal (short vs. long delay) aspects of sensorimotor interactions. Two consecutive electrocutaneous stimuli (separated by either 30 or 125 ms) were delivered to either the same or different fingers on the left hand (i.e. index finger stimulated twice or middle finger stimulated before index finger). Information about which fingers were stimulated was reflected in the size of the motor responses in a time-constrained manner: CSE was modulated differently by same and different finger stimulation only when the two stimuli were separated by the short delay (P = 0.004). We demonstrate that the well-known response of the somatosensory cortices following repetitive stimulation is mirrored in the motor cortex and that CSE is modulated as a function of the temporal and spatial relationship between afferent stimuli. © 2015 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
    Full-text · Article · Mar 2015 · European Journal of Neuroscience
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    • "More medial areas in vM1 are devoid of tactile responses (Gerdjikov et al., 2013; Smith and Alloway, 2013). The connection between vS1 and vM1 is reciprocal with the vM1-vS1 projection arising mainly from layers II/III and Va and targeting preferentially the deeper layers but also layer I as well as the septal regions in Layer IV in vS1 (Sato and Svoboda, 2010; Mao et al., 2011; Petreanu et al., 2012; Zagha et al., 2013; Kinnischtzke et al., 2014). The vM1 projections to vS1 primarily target VIP expressing interneurons in vS1 resulting in whisking related modulation of vS1 activity (Lee et al., 2013). "

    Full-text · Article · Jan 2015
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