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J R Fetcho

Publications and source records attributed to J R Fetcho.

25 records · Page 2Linked to original sources

Spinal network of the Mauthner cell.

Most swimming vertebrates, particularly fishes and amphibians, avoid predators by producing an escape behavior initiated by a single action potential in one of a pair of cells, the Mauthner cells, located in the hindbrain. The most prominent feature of this behavior is a rapid, forceful bend of body and tail which leads to a characteristic C bend (stage 1) early in the escape. The spinal output of the Mauthner cell is largely responsible for this bend. Each Mauthner cell sends an axon down the length of the spinal cord on the side opposite the soma. When one Mauthner axon fires, it massively excites the ipsilateral musculature by (1) monosynaptic excitation of the large primary motoneurons that innervate the fast white muscle fibers and (2) polysynaptic excitation of motoneurons which is most likely mediated through an identified class of descending interneurons. While motoneurons on the side of the C bend are excited, excitation of those on the opposite side is blocked by inhibition of primary motoneurons and descending interneurons. This inhibition is mediated by commissural interneurons that are electrotonically coupled to the Mauthner axon and cross the spinal cord to monosynaptically inhibit cells on the opposite side. They inhibit not only primary motoneurons and descending interneurons, but also the commissural inhibitory interneurons on the opposite side. The inhibition of contralateral primary motoneurons and descending interneurons prevents motor activity on the side opposite the C bend from opposing that bend, while the inhibition of commissural interneurons prevents them from interfering, via their inhibitory connections, with excitation of motoneurons on the side of the bend. The spinal network responsible for the bend has several similarities with the spinal network for swimming in other anamniotic vertebrates, including lampreys and embryonic frogs. These similarities reveal important, primitive features of axial motor networks among vertebrates.

Animals↗

Morphological variability, segmental relationships, and functional role of a class of commissural interneurons in the spinal cord of goldfish.

As part of an attempt to understand the spinal control of the segmented axial musculature in goldfish, commissural spinal interneurons that are electronically coupled to the Mauthner axon (M-axon) were studied with intracellular recording and staining to examine their morphology, segmental relationships, and functional role. Prior studies suggested that these cells might mediate the crossed inhibition that blocks excitation of motoneurons on one side of the body during an escape bend to the opposite side. Simultaneous intracellular recordings from a M-axon, a commissural interneuron coupled to it, and a presumed primary motoneuron show that: (1) the interneurons produce monosynaptic, Cl(-)-dependent IPSPs in contralateral motoneurons, (2) the interneurons are responsible for the short latency, crossed spinal inhibition in the M-cell network, and (3) more than one interneuron terminates on each postsynaptic cell. Reconstructions of interneurons from wholemounts show that they form a fairly homogeneous morphological class of cells. Each one is unipolar, with an axon that crosses the cord and then usually bifurcates into a short, thin ascending branch and a thicker, longer descending one. Neighboring interneurons have overlapping terminal arbors consistent with the physiological data showing convergence of interneurons onto the same postsynaptic cell. The interneurons showed little relationship with body segments as defined by ventral roots. Their axons usually straddled segmental boundaries, with terminals typically occupying parts of two adjacent segments. Thus the functional unit of these cells is probably not a segment or a complete group of segments, but instead includes only parts of two adjacent segments. The presence of interneurons like these suggests that the overt peripheral segmentation of trunk musculature is not necessarily reflected in the organization of neurons that control those segments. A consideration of some functional characteristics of the activation of overlapping, serially repeated arrays of interneurons by descending pathways leads to the conclusion that the high conduction velocity of the M-axon, and the large size and short longitudinal extent of the axons of the inhibitory interneurons promote a strong, brief inhibition that is appropriate for the production of an escape turn that has a rapid bend to one side.

Animals↗

Identification of motoneurons and interneurons in the spinal network for escapes initiated by the mauthner cell in goldfish.

We used intracellular recording and staining techniques to study the spinal circuitry of the escape behavior (C-start) initiated by the Mauthner axon (M-axon) in goldfish. Simultaneous intracellular recordings from one or both M-axons and a spinal neuron, followed by HRP labeling of the spinal cell, show that each M-axon makes monosynaptic, chemical excitatory synapses onto 2 populations of ipsilateral spinal neurons. The first consists of the large primary motoneurons that, based on earlier work (Fetcho, 1986), innervate exclusively the faster, white muscle fiber types in the myomeres. The second group of cells is formed by previously undescribed descending interneurons with ipsilateral axonal branches that have contacts with primary and secondary motoneurons spread over 2 or more body segments. Indirect evidence suggests that these descending interneurons are excitatory, and they may explain the polysynaptic activation of motoneurons observed in earlier studies of the spinal circuitry (Diamond, 1971). Both classes of neurons excited by the ipsilateral M-axon are disynaptically inhibited by the contralateral one. The morphology and physiology indicate that this inhibition is mediated by interneurons that are electrotonically coupled to one M-axon and have processes that cross the cord to inhibit contralateral neurons in the region where these postsynaptic cells receive excitatory input from the other M-axon. We have identified interneurons with the physiological and morphological features of these predicted crossed inhibitory interneurons. These cells are electrotonically coupled to the ipsilateral M-axon and receive a chloride-dependent disynaptic inhibitory input from the contralateral M-axon. Their very simple somata give rise to a process that crosses the spinal cord between the 2 M-axons. Once on the opposite side of the cord, the crossing process sends myelinated branches that run rostrally and caudally, roughly parallel to the contralateral M-axon. Processes that arise from these longitudinal branches terminate in a striking association with collaterals of the M-axon; nearly every M-axon collateral along the longitudinal course of an interneuron is met by a branch or branches of the interneuron whose terminals are apposed to neurons postsynaptic to the collateral.(ABSTRACT TRUNCATED AT 400 WORDS)

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A review of the organization and evolution of motoneurons innervating the axial musculature of vertebrates.

In most anamniotes the axial musculature is myomeric and is functionally subdivided into superficial red and deep white muscle. In those anamniotes that have been studied the organization of the motor column is related to this functional subdivision. The motoneurons innervating red and white muscle differ in size, distribution in the motor column, and developmental history. There is no obvious topographic relationship between the location of motoneurons in the motor column and the dorsoventral location of the muscle they innervate in the myomeres; epaxial motoneurons are not segregated from hypaxial ones. Among amniotes, the myomeres divide to form a number of discrete muscles that may be complexly arranged. This breakup of the musculature is correlated with a subdivision of the motor column into discrete motor pools serving the different muscles. Unlike anamniotes, the motor pools are topographically organized. The epaxial pools are segregated from hypaxial ones, and within the epaxial and hypaxial pools the location of motoneurons innervating any particular muscle is related to the location of the muscle's precursor in the embryonic muscle masses. Thus adjacent motor pools innervate muscles arising from adjacent positions in the myotome. These dramatic differences between the motor columns in anamniotes and amniotes imply that the medial motor column has undergone a major restructuring during the evolution of vertebrates. The available evidence--which is tentative because of the few species that have been studied--suggests that a topographically organized motor column was absent in early vertebrates. A motor column/myotome map appears to have arisen just prior to, or in conjunction with the origin of amniotic vertebrates. The details of this map were conserved in different amniotes in spite of major structural and functional changes in the musculature. The map may be important for the proper control of the many muscles arising from the myotomes in amniotes because it facilitates the development and evolution of motor systems in which anatomically and functionally different muscles have spatially separate motor pools in the cord.

Animals↗

The organization of the motoneurons innervating the axial musculature of vertebrates. I. Goldfish (Carassius auratus) and mudpuppies (Necturus maculosus).

The motoneurons innervating different regions of the myomeres in goldfish and mudpuppies were examined by applying HRP to the musculature or to branches of spinal nerves. In goldfish, the populations of motoneurons innervating epaxial or hypaxial muscle occupied similar positions in the motor column and had similar size distributions. There was no relationship between the size or location of a motoneuron in the motor column and the dorsoventral location of the muscle it innervated in the myomeres. Instead, different populations of motoneurons innervated the functionally different red and white musculature. The red muscle was innervated only by small motoneurons that occupied the ventral portion of the motor column. Their small axons passed lateral to the Mauthner axon in the cord, and most of them traveled in a separate branch of each spinal nerve that ran in the horizontal septum to the red muscle. The white muscle was innervated by a population of motoneurons that did not innervate red. They were large and they occupied a characteristic position in the extreme dorsal part of the motor column. Their large axons traveled medial to the Mauthner axon in the cord and entered branches of spinal nerves running deep in the epaxial or hypaxial muscle. The white muscle was probably also innervated by some smaller motoneurons similar to those innervating red; however, these may have been motoneurons whose axons ran through white muscle to reach other muscle. The large motoneurons innervating only white muscle are similar to the primary motoneurons identified in developmental studies in teleosts (Myers: Soc. Neurosci. Abstr. 9:848, '83); the smaller ones, innervating both red and white, are like secondary motoneurons. Therefore, in goldfish, motoneurons having different morphology and developmental history also innervate different regions in the myomeres. The motor column in mudpuppies was, in general respects, similar to the column in goldfish. There were large primary motoneurons and small secondary ones. Though there were slight differences in the locations of motoneurons filled from nerves entering epaxial and hypaxial muscle, their distributions in the cord overlapped substantially. The motor columns in these two anamniotes differ substantially from the motor columns in those amniotes that have been studied. In amniotes, the motoneurons innervating epaxial and hypaxial muscles are spatially segregated in the cord (Smith and Hollyday: J. Comp. Neurol. 220:16-28, '83; Fetcho: J. Comp. Neurol. 249:551-563, '86).(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

The organization of the motoneurons innervating the axial musculature of vertebrates. II. Florida water snakes (Nerodia fasciata pictiventris).

The motor pools of axial muscles in Florida water snakes (Nerodia fasciata pictiventris) were studied by applying horseradish peroxidase (HRP) to branches of spinal nerves innervating individual muscles or groups of muscles. Motor pools of different muscles or muscle groups were located in characteristic positions in both the transverse and the longitudinal extent of the motor column. Epaxial pools were located ventromedially in the column, segregated from most hypaxial ones, which were dorsolateral. The only exception to this general rule was the motoneurons innervating the levator costae muscle. Some of the motoneurons innervating this hypaxial muscle were located in the ventral part of the motor column, like epaxial motoneurons, but they were segregated longitudinally from epaxial ones. The arrangement of the motor pools was strikingly similar to the motor pools of presumptive homologous muscles in rats (Smith and Hollyday: J. Comp. Neurol. 220:29-43, '83), even though the locomotor mechanics in the two animals are very different. The similarities may reflect a comparable relationship between the location of motoneurons in the motor column and the location, in embryonic life, of the muscles they innervate. They also suggest that differences in the locomotor mechanics in the two species are accomplished without any dramatic reorganization of the medial motor column, in marked contrast to the substantial reorganization necessary to account for differences in the motor columns of amniotes and anamniotes.

Afferent Pathways↗