Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord

Li, W.-C.; Higashijima, Shin‐ichi; Parry, DM; Roberts, Alan; Soffe, Stephen R

doi:10.1523/jneurosci.1633-04.2004

Cited by 105 publications

(144 citation statements)

References 38 publications

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“…The dINs in turn excite all CPG neurons on their own side (Li et al, 2006). The other CPG neurons are aINs, which provide ipsilateral, recurrent inhibition (Li et al, 2004d), cINs, which provide contralateral, reciprocal inhibition (Dale, 1985;Soffe et al, 2001) and MNs, which connect to the muscles and cause the swimming movements (Soffe and Roberts, 1982).…”

Section: Activity Of Spinal Neurons-network Diagrammentioning

confidence: 99%

“…We know that, in addition, aINs provide recurrent inhibition to CPG neurons (Li et al, 2004d), and this inhibition is particularly prominent as swimming is initiated.…”

Section: Importance Of Ains In the Swimming Networkmentioning

confidence: 99%

“…These include: their passive and active responses to current injection, the transmitter pharmacology of synapses they make and receive (where some synaptic conductances have been studied in voltage-clamp recordings), and their activity during responses to sensory stimuli. Such detailed information has shown that 7 of the anatomical classes correspond to distinct functional classes: 1 type of sensory neuron innervating the skin (Clarke et al, 1984;Li et al, 2003); 2 types of sensory pathway neuron that have a role in the initiation of swimming (Li et al, 2003(Li et al, , 2004b; 3 types of premotor neuron that are active during swimming and may be components of the swimming central pattern generator (Dale, 1985;Li et al, 2002Li et al, , 2004dLi et al, , 2006; and motoneurons (Soffe and Roberts, 1982;Roberts et al, 1999). These detailed studies have recently provided evidence of functional sub-types within two anatomical classes (Li et al, unpublished).…”

Section: Introductionmentioning

confidence: 99%

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Role of type-specific neuron properties in a spinal cord motor network

Sautois

Soffe

et al. 2007

J Comput Neurosci

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Recent recordings from spinal neurons in hatchling frog tadpoles allow their type-specific properties to be defined. Seven main types of neuron involved in the control of swimming have been characterized. To investigate the significance of type-specific properties, we build models of each neuron type and assemble them into a network using known connectivity between: sensory neurons, sensory pathway interneurons, central pattern generator (CPG) interneurons and motoneurons. A single stimulus to a sensory neuron initiates swimming where modelled neuronal and network activity parallels physiological activity. Substitution of firing properties between neuron types shows that those of excitatory CPG interneurons are critical for stable swimming. We suggest that type-specific neuronal properties can reflect the requirements for involvement in one particular network response (like swimming), but may also reflect the need to participate in more than one response (like swimming and slower struggling).

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Section: Activity Of Spinal Neurons-network Diagrammentioning

confidence: 99%

“…We know that, in addition, aINs provide recurrent inhibition to CPG neurons (Li et al, 2004d), and this inhibition is particularly prominent as swimming is initiated.…”

Section: Importance Of Ains In the Swimming Networkmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Role of type-specific neuron properties in a spinal cord motor network

Sautois

Soffe

et al. 2007

J Comput Neurosci

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“…Some could correspond to dorsal group 4 parvalbumin immunoreactive neurons. Alternatively, dorsal V1-dervied parvalbumin neurons might include additional types of proprioceptive interneurons derived from the V1 group.It is interesting that in tadpoles and zebrafish En1 expression also defines a unique subpopulation of glycinergic interneurons that provides both recurrent and reciprocal inhibition to motoneurons and gates sensory pathways that modulate swimming Li et al, 2004). Moreover, neurons with synaptic properties that are intermediate between Renshaw cells and proprioceptive inhibitory interneurons like the IaINs, were also described in chick embryos (Wenner et al, 1999).…”

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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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“…These canonical embryonic interneurons and their primary characteristics are conserved phylogenetically, but interestingly, the number and types of neurons derived from each class increases in complexity in parallel with the evolution of locomotion from fish to terrestrial animals (reviewed in Grillner and Jessell, 2009). V1-interneurons in zebrafish and tadpoles constitute a rather homogenous population that gates sensory-motor responses and are more effectively recruited at higher locomotor speeds Li et al, 2004). In mammals, however, they give rise to several different types of adult premotor inhibitory interneurons with different functions .…”

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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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Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord

Cited by 105 publications

References 38 publications

Role of type-specific neuron properties in a spinal cord motor network

Role of type-specific neuron properties in a spinal cord motor network

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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