Central Pathway for Direct Inhibitory Action of Impulses in Largest Afferent Nerve Fibres to Muscle

Eccles, John C.; Fatt, P.; Landgren, S.

doi:10.1152/jn.1956.19.1.75

Cited by 243 publications

(154 citation statements)

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“…Despite this shared embryonic origin, each interneuron subtype differs in its pattern of synaptic connections in the adult. IaINs receive input from Ia muscle afferents and mediate reciprocal inhibition between antagonistic motor pools, but they lack direct input from motoneurons (Eccles et al, 1956). In contrast, Renshaw cells mediate recurrent inhibition of homonymous and synergistic motoneurons and have been assumed to lack monosynaptic input from primary afferents (Renshaw 1946;Eccles et al, 1954).…”

Section: Introductionmentioning

confidence: 99%

Primary Afferent Synapses on Developing and Adult Renshaw Cells

Mentis¹,

Siembab²,

Zerda³

et al. 2006

J. Neurosci.

108

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Section: Introductionmentioning

confidence: 99%

Primary Afferent Synapses on Developing and Adult Renshaw Cells

Mentis¹,

Siembab²,

Zerda³

et al. 2006

J. Neurosci.

108

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“…These studies, which relied heavily on the physiological identification of synaptic inputs and (Renshaw 1946;Eccles et al, 1954). IaINs are characterized by inputs from sensory Ia muscle afferents, provide reciprocal inhibition to antagonistic motor pools (Eccles et al, 1956) and are modulated by RCs (Hultborn et al, 1971). Despite enormous progress in further identification of interneurons using these methods, much is unknown and this approach is not without limitations (Edgley, 2001;Jankowska, 2001).…”

mentioning

confidence: 99%

Postnatal phenotype and localization of spinal cord V1 derived interneurons

Álvarez

Jonas

Sapir

et al. 2005

J of Comparative Neurology

226

284

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Developmental studies identified four classes (V0, V1, V2, V3) of embryonic interneurons in the ventral spinal cord. Very little however is known about their adult phenotypes. In order to further characterize interneuron cell types in the adult, the location, neurotransmitter phenotype, calciumbuffering protein expression and axon distributions of V1-derived neurons in the mouse spinal cord was determined. In the mature (P20 and older) spinal cord, most V1-derived neurons are located in lateral LVII and in LIX, few in medial LVII and none in LVIII. Approximately 40% express calbindin and/or parvalbumin, while few express calretinin. Of seven groups of ventral interneurons identified according to calcium-buffering protein expression, two groups (1 and 4) correspond with V1-derived neurons. Group 1 are Renshaw cells and intensely express calbindin and coexpress parvalbumin and calretinin. They represent 9% of the V1 population. Group 4 express only parvalbumin and represent 27% of V1-derived neurons. V1-derived group 4 neurons receive contacts from primary sensory afferents and are therefore proprioceptive interneurons and the most ventral neurons in this group receive convergent calbindin-IR Renshaw cell inputs. This subgroup resembles Ia inhibitory interneurons (IaINs) and represents 13% of V1-derived neurons. Adult V1-interneuron axons target LIX and LVII and some enter the deep dorsal horn. V1-axons do not cross the midline. V1 derived axonal varicosities were mostly (>80%) glycinergic and a third were GABAergic. None were glutamatergic or cholinergic. In summary, V1 interneurons develop into ipsilaterally projecting, inhibitory interneurons that include Renshaw cells, Ia inhibitory interneurons and other unidentified proprioceptive interneurons.Keywords inhibitory interneurons; engrailed-1; motor control; GABA; glycine; calbindin; parvalbumin; calretinin; motoneurons; ventral horn; spinal cord; development; V1 During the past 50 years, classical studies in the spinal cord have uncovered a wealth of details about the organization of interneuronal networks that control motoneuron firing, segmental reflexes and generate locomotor patterns in mammals (Jankowska et al., 1992). These studies, which relied heavily on the physiological identification of synaptic inputs and (Renshaw 1946;Eccles et al., 1954). IaINs are characterized by inputs from sensory Ia muscle afferents, provide reciprocal inhibition to antagonistic motor pools (Eccles et al., 1956) and are modulated by RCs (Hultborn et al., 1971). Despite enormous progress in further identification of interneurons using these methods, much is unknown and this approach is not without limitations (Edgley, 2001;Jankowska, 2001). Thus a comprehensive classification of ventral interneurons into major subclasses has not yet emerged.Recent studies indicate that distinct cell types in the adult spinal cord are derived from genetically-discrete populations of embryonic neurons (Jessell, 2000;Briscoe and Ericson, 2001;Lee and Pfaff, 2001;Goulding et al., 2002, Sa...

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“…Adult RCs mediate recurrent inhibition of homonymous and synergistic motoneurons and receive strong excitatory drive from recurrent collaterals of motor axons (Eccles et al, 1954; reviewed in Alvarez and Fyffe 2007). In contrast, IaINs mediate reciprocal inhibition between antagonistic motor pools and receive strong excitation from Ia afferents (Eccles et al, 1956;Jankowska and Roberts, 1972;Jankowska and Lindstrom, 1972; Rastad et al, 1990). The different sources of excitatory drive places each interneuron in a different functional position within the motor network and also serves as a method of identification.…”

mentioning

confidence: 99%

Target selection of proprioceptive and motor axon synapses on neonatal V1‐derived Ia inhibitory interneurons and Renshaw cells

Siembab

Smith

Zagoraiou

et al. 2010

J of Comparative Neurology

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The diversity of premotor interneurons in the mammalian spinal cord is generated from a few phylogenetically conserved embryonic classes of interneurons (V0, V1, V2, V3). Their mechanisms of diversification remain unresolved, although these are clearly important to understand motor circuit assembly in the spinal cord. Some Ia inhibitory interneurons (IaINs) and all Renshaw cells (RCs) derive from embryonic V1 interneurons; however, in adult they display distinct functional properties and synaptic inputs, for example proprioceptive inputs preferentially target IaINs, while motor axons target RCs. Previously, we found that both inputs converge on RCs in neonates, raising the possibility that proprioceptive (VGLUT1-positive) and motor axon synapses (VAChT-positive) initially target several different V1 interneurons populations and then become selected or deselected postnatally. Alternatively, specific inputs might precisely connect only with predefined groups of V1 interneurons. To test these hypotheses we analyzed synaptic development on V1-derived IaINs and compared them to RCs of the same age and spinal cord levels. V1-interneurons were labeled using genetically encoded lineage markers in mice. The results show that although neonatal V1-derived IaINs and RCs are competent to receive proprioceptive synapses, these synapses preferentially target the proximal somato-dendritic regions of IaINs and postnatally proliferate on IaINs, but not on RCs. In contrast, cholinergic synapses on RCs are specifically derived from motor axons, while on IaINs they originate from Pitx2 V0c interneurons. Thus, motor, proprioceptive, and even some interneuron inputs are biased toward specific subtypes of V1-interneurons. Postnatal strengthening of these inputs is later superimposed on this initial preferential targeting. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptThe development of spinal cord local interneuronal circuits is currently poorly understood. Recent work has defined a relatively small number of cardinal interneurons in embryo that generates the much larger diversity of adult interneurons (Goulding, 2009). In the ventral horn just four embryonic subgroups (V0, V1, V2, V3) generate most adult premotor interneurons by diversification mechanisms that are currently largely unknown. Each group displays common properties that generally include origins from one type of progenitor cell (p0, p1, p2, p3), the direction taken by the primary axon, their cell migration and final location in the ventral horn with relation to motor pools, and their neurotransmitter phenotype. For example, V1 interneurons have common origins in the p1 progenitor area and are characterized by expression of the engrailed-1 (En-1) transcription factor. They migrate ventrolaterally, positioning themselves adjacent to motor pools, extend ascending axons that target ipsilateral motoneurons, and have an inhibitory phenotype (Matise and Joyner, 1997; Ericsson et al., 1997;Saueressig et al., 1999;Sapir et al., 2004;Alvarez et a...

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Central Pathway for Direct Inhibitory Action of Impulses in Largest Afferent Nerve Fibres to Muscle

Cited by 243 publications

References 0 publications

Primary Afferent Synapses on Developing and Adult Renshaw Cells

Primary Afferent Synapses on Developing and Adult Renshaw Cells

Postnatal phenotype and localization of spinal cord V1 derived interneurons

Target selection of proprioceptive and motor axon synapses on neonatal V1‐derived Ia inhibitory interneurons and Renshaw cells

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