Descending propriospinal axons in the hindlimb enlargement of the red‐eared turle: Cells of origin and funicular courses

Abstract

Spinal neurons with descending axons are important components of spinal sensorimotor networks. We used an anatomical tracing technique to study the distribution of descending propriospinal axons and cell bodies in red-eared turtles. We injected horseradish peroxidase into a portion of one funiculus in the middle of the hindlimb enlargement and examined six spinal segments rostral to the injection site (dorsal 3 through dorsal 8) for labeled neuronal cell bodies. Injections into each region of the white matter labeled substantial numbers of descending propriospinal neurons. Each injection labeled cell bodies over most of the six spinal segments examined. Each injection also labeled cell bodies in the ipsilateral dorsal horn, intermediate zone, and ventral horn as well as the contralateral intermediate zone and ventral horn. Injections into each of four regions of the white matter, the dorsal funiculus, the medial part of the lateral funiculus, the lateral part of the lateral funiculus, and the ventral funiculus reliably gave rise to a distinct distribution of labeled cell bodies. These experiments establish that descending propriospinal axons in red-eared turtles are found in all regions of the spinal white matter. This finding contrasts with a popular contemporary view of the organization of descending propriospinal axons in mammals. These experiments also demonstrate that neurons in each region of the gray matter give rise to a different distribution of descending, funicular axons, although these distributions are widely overlapping. Different funicular axon distributions could be associated with different sets of synaptic contacts with the white-matter dendrites of spinal neurons.

Somato-Dendritic Morphology Predicts Physiology for Neurons That Contribute to Several Kinds of Limb Movements

“…Motoneurons, having unusually large somata and unusually complex dendritic trees (McDonagh et al 1998(McDonagh et al , 2002, may require either simultaneous inputs from a large number of premotor interneurons or inputs from rhythmic premotor interneurons that have especially high peak firing rates, as T cells do. Second, T cells, having dendrites that extend far into the lateral funiculus and ventral funiculus, are positioned to receive and integrate inputs from a wide variety of ascending and descending propriospinal and descending brain sources that are known to modulate hindlimb motor patterns (Drew et al 2004;Grillner and Dubuc 1988;Orlovsky et al 1999) and may make en passant synapses within the white matter (Berkowitz and Stein 1994b). Third, T cells have small somata that are easily driven beyond action potential threshold, which may allow their inputs to be especially effective in driving them.…”

“…The strongly rhythmic activity of T cells during multiple forms of scratching bilaterally and activity typically during withdrawal as well is consistent with their being a subset of "scratch/swim neurons," which are activated during scratching, forward swimming, and often additional hindlimb motor patterns (Berkowitz 2002); however, tests of this prediction will have to await a further set of experiments in a preparation that also produces swimming motor patterns. T cell somata are distributed similarly to those of descending propriospinal neurons (Berkowitz and Stein 1994b). The strongly rhythmic activity of T cells and their predominantly ventral soma locations may partly account for the previously observed correlation between depth and rhythmicity of scratchactivated spinal interneurons (Berkowitz 2001b).…”

Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: phase analyses

“…This finding is somewhat surprising, because studies of scratching have generally focused on ipsilateral neural circuitry. On the other hand, there are many propriospinal neurons with descending crossed axons in turtles (Kusuma and ten Donkelaar, 1980;Berkowitz and Stein, 1994a), as well as in lampreys (Buchanan, 1982;Ohta et al, 1991), embryonic tadpoles (see Roberts, 1989) embryonic newts (Harper and Roberts, 1993) goldfish (Fetcho, I99 1), lizards (ten Donkelaar and de Boer van Huizen, 1978;Kusuma and ten Donkelaar, 1980) chicks (Oppenheim et al, 1988) and mammals (Burton and Loewy, 1976;Molenaar, 1978;Molenaar and Kuypers, 1978;Matsushita et al, 1979;Menetrey et al, 1985;Hongo et al, 1989;Cassidy and Cabana, 1993). In addition, during turtle fictive scratching evoked by unilateral tactile stimulation, some hindlimb muscle nerves on the opposite side of the body are often activated with a clear rhythm ( Fig.…”

Dendritic orientation and branching distinguish a class of multifunctional turtle spinal interneurons

“…Descending propriospinal axons have been shown to have swellings within the lateral funiculus (Berkowitz and Stein, 1994), suggesting that they make en passant synapses onto local dendrites. T neuron dendrites in the lateral and ventral funiculi may receive funicular axonal en passant synaptic inputs from multiple sources, including propriospinal axons from other segments and supraspinal descending axons.…”

“…Propriospinal axons, at least, make putative en passant synapses in the lateral funiculus in addition to terminal arbors in the gray matter (Berkowitz and Stein, 1994). But distally generated postsynaptic potentials would be greatly attenuated at the soma unless dendritic characteristics opposed such attenuation (Segev and London, 2000; Williams and Stuart, 2002, 2003; Gulledge et al, 2005).…”