Neural architectures for adaptive behavior

doi:10.1016/0166-2236(94)90015-9

Trends in Neurosciences

Volume 17, Issue 10, 1994, Pages 413-420

https://doi.org/10.1016/0166-2236(94)90015-9 Get rights and content

Abstract

How do animals use the same peripheral structures to generate different behavioral responses? Three different neuronal architectures have been proposed to mediate this task: dedicated circuitry; distributed circuitry; and reorganizing circuitry. This review will critically examine the evidence for these different architectures in invertebrate circuits, and then examine the evidence for them in more complex vertebrate circuits. The evidence suggests that these different architectures are unlikely to be found in pure form in most neural circuits, but are useful for guiding the experimental analysis of circuitry.

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Studies on Aplysia feeding have provided insight into a number of principles of neural organization. For example, it has contributed to an understanding of how multiple behaviors are generated by a single neural circuit controlling a set of muscles (Chiel, 2007; Hurwitz et al., 1997; Jing and Weiss, 2001, 2002; Morgan et al., 2002; Morton and Chiel, 1994; Proekt et al., 2007; Sasaki et al., 2008). Shifting coalitions of muscles and motor neurons generate different behaviors, which can be understood within a biomechanical context (Chiel et al., 2009).
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To generate the multiple motor patterns, distinct anatomical circuits of neurons can operate in more than one stable mode, and their connectivity can switch between functional activity patterns under various conditions. These polymorphic neuronal circuits have been referred to as ‘reorganizing circuits’ (Morton and Chiel, 1994) or ‘multifunctional circuitry’ (Kristan et al., 1988). Most of studies of the multifunctional circuitry have focused on rhythmic movements and their underlying CPG (Grillner, 2006; Kiehn, 2006; Marder, 2000; Marder and Bucher, 2001).
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The term locomotion covers a series of named stereotypical patterns (walking, jogging, running, etc.), while the pattern of mastication varies not only between foods but also from the beginning to the end of a single sequence of movements (Peyron et al., 2002; Woda et al., 2006). The ways in which CPGs generate distinct patterns of motoneuron firing has been exhaustively investigated in invertebrates and lower vertebrates, and evidence has been found for three basic CPG structures: dedicated circuits, distributed circuits, and reorganizing circuits (Morton and Chiel, 1994). We decided to investigate this in our rabbit mastication model.
The main text of this chapter, written by James P. Lund, summarizes most of the work related to the neural control of mastication that he conducted with his collaborators throughout the years. From his early PhD work showing that mastication is centrally patterned to his latest work related to the interaction between pain and movement, Lund will have addressed many essential questions regarding the organization and functioning of the masticatory central pattern generator (CPG). His earliest studies examined how the CPG modulates reflexes and the excitability of primary afferents, interneurons, and motoneurons forming their circuitry. He then tackled the question of how the CPG itself was modulated by different types of sensory and cortical inputs. Another series of studies focused on the organization of the subpopulations of neurons forming the CPG, their intrinsic and network properties. Shortly before his untimely passing, he had turned his attention to the potential contribution of muscle spindle afferents to the patterning of mastication as well as to the development of chronic muscle pain.
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Citation Excerpt :
Mass activation can be used in principle to determine such motor parameters as pitch, roll and turn direction, and might easily be extended to the control of bend amplitude and tail-beat frequency via increasing synaptic excitation (Hill et al., 2005; Knudsen et al., 2006). Such a scheme would fall within the “distributed” neural architecture from Morton and Chiel's (1994) classifications of distributed, dedicated and reorganizing motor networks, but there are questions about “distributed motor control” even in lamprey, where the descending projections to each quadrant of spinal cord (left, right, upper and lower) are heterogeneous, being comprised of at least 20 distinct cell types in total (Zelenin et al., 2001). Given this diversity of physiological-anatomical cell types, one may need to think in terms of “dedicated circuits” whereby sets of cell types produce specific motor outputs.
Action potentials from the brain control the activity of spinal neural networks to produce, by as yet unknown mechanisms, a variety of motor behaviors. Particularly lacking are details on how identified descending neurons integrate diverse sensory inputs to generate specific locomotor patterns. We have examined the operations of the principal neurons in an intriguing midbrain nucleus, the nucleus of the medial longitudinal fasciculus (nMLF), in the larval zebrafish. The nMLF is the most rostral grouping of neurons that projects from the brain well into the spinal cord of teleost fishes, yet there is little direct physiological data available regarding its function. We report here that a distinct set of large, individually-identifiable neurons in nMLF (the MeL and MeM neurons) are activated by diverse sensory stimuli and contribute to distinct locomotor behaviors. Using in vivo confocal calcium imaging we observed that both photic and mechanical stimuli elicit calcium responses indicative of the firing of action potentials. Calcium responses were observed simultaneously with distinct swimming, turning and struggling movements of the larval trunk. While selectively contralateral responses were at times observed in response to a head-tap stimulus, these nMLF cells showed roughly similar numbers of bilateral responses. Calcium responses were observed at a range of latencies, suggesting involvement with both slow swimming patterns and the burst swimming component of the escape behavior. The MeL cells in particular were strongly activated during light-evoked slow swimming. The activation of MeL cells during the slow and burst forward swim gaits is consistent with their driving and/or coordinating the activity of slow and fast central pattern generators in spinal cord. As such, the MeL cells may help to shape a variety of larval behaviors including the optomotor response, escape swimming and prey capture.

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Trends in Neurosciences

ReviewNeural architectures for adaptive behavior

Abstract

Trends Neurosci.

J. Insect Physiol.

Annu. Rev. Neurosci.

J. Neurosci.

J. Neurophysiol.

J. Comp. Physiol. A

Science

J. Neurosci.

J. Neurobiol.

J. Exp. Biol.

J. Neurophysiol.

J. Neurophysiol.

J. Neurophysiol.

J. Neurophysiol.

Review
Neural architectures for adaptive behavior