Learning in sensorimotor circuits

University of Bristol (2005) J Physiol 567P, SA17

Research Symposium: Learning in sensorimotor circuits

Schouenborg, Jens;

1. Section for Neuroscience, Exp Medical Science, Lund, Sweden.

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The study of plasticity in CNS is a major and very dynamic neuroscience research field with enormous clinical potentials. It now appears that most circuits in the brain and spinal cord show plasticity and that they can be modified by experience. Understanding the mechanisms of plasticity in the nervous system is therefore essential for the understanding of how the nervous system is wired during development and how it adapts in response to changes in the body and environment. This lecture focuses on self-organizing adaptive plasticity in spinal sensorimotor circuits. To be useful in motor control, somatosensory information must be encoded (weighted) with respect to body anatomy and movement patterns produced by the sensorimotor circuits. This is a difficult task since the multisensory information (nociception, pressure, temperature, joint angles, muscle force and length) arises from a complex body constitution. The information processing that needs to be performed is therefore staggering. Understanding how the basic sensorimotor system functions are adapted to the body anatomy and biomechanics is therefore a major task. To understand the cellular mechanisms underlying functional adaptation in the spinal cord, knowledge on the functional organization of the neural circuits is essential. During the last 10 years the concept of a modular organization of the spinal cord has grown stronger. A modular type of reflex organisation in the mammalian spinal cord was first demonstrated for the nociceptive withdrawal reflex (NWR) system. In this system, each excitatory module preferentially acts on a single muscle and performs a detailed sensorimotor transformation resulting in a graded withdrawal of the limb (or part of the limb) from its receptive field. For each excitatory NWR module, the input strength has a characteristic pattern on the skin that mimics the pattern of withdrawal efficacy when the output muscle of the module contracts. In a sense, the pattern of withdrawal efficacy is imprinted on the receptive field of the module. A corresponding set of inhibitory reflex modules also exists. In this case, the receptive fields correspond to the graded movement of the skin area towards external stimulation (i.e. increase in load) on contraction of the muscle in the module. As a result of this organisation, the excitatory and inhibitory modules are engaged to a degree that is proportional to their respective withdrawal/loading efficacy on skin stimulation. Given that the adult sensorimotor transformations performed by the spinal cord reflect precisely weighted connections in modules – how can this weighting be achieved during development? Previous studies in this laboratory have shown that an experience dependent mechanism termed somatosensory imprinting underlies the functional adaptation of this system. Recently, we found that tactile feedback ensuing on spontaneous motility in spinal sensorimotor circuits is used to tune the connection strengths in nociceptive withdrawal reflex modules during postnatal development in the rat. Thus, tactile inputs from the skin area normally withdrawn and arriving in conjunction with the spontaneous movements had an adaptive effect on the reflex modules. This learning took place over postnatal days 12-17. Uncorrelated input (given at random time points) did not cause a learning effect. Since this process results in an imprint of the withdrawal efficacy on the reflex modules, it was termed motor directed sensorimotor imprinting (MDSI). Notably this novel form of unsupervised learning occurs during active sleep, characterized by atonia in the musculature. This state may be particularly advantageous for learning since the sensory feedback on muscle contraction stands out from a more or less silent background. Spontaneous movements are a ubiquitous phenomenon during embryonic development in all vertebrates and mammals. Their role in sensorimotor learning has, however, not been known. The activity appears to be caused by spontaneous endogenous activity in neuronal circuits the spinal cord and brain stem. Although present classifications tend to lump the spontaneous motility broadly into a few categories, detailed studies in humans have distinguished up to 16 different types. The prevalence and complexity of these movements lead us to suggest that all major spinal motor systems contribute to the spontaneous movements during development. Furthermore, since this adaptive learning is highly effective, it may well be that all major groups of spinal motor systems learn relevant aspects of the body anatomy and biomechanics during development by probing the sensory feedback after spontaneous endogenous activation.



Where applicable, experiments conform with Society ethical requirements.

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