Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology

Abstract

1. As part of a continuing investigation of the organization of the spinal cord of the lamprey, propriospinal interneurons with axons projecting contralaterally and caudally (CC interneurons) were surveyed with intracellular recordings. 2. CC interneurons were identified by recording their axon spikes extracellularly in the spinal cord during intracellular stimulation of the cell body. The axon projections of Cc interneurons were confirmed after intracellular injection and development of horseradish peroxidase. 3. Intracellular stimulation of CC interneurons produced synaptic potentials in myotomal motoneurons, lateral interneurons and other CC interneurons that lay caudally on the opposite side of the spinal cord. Most CC interneurons were inhibitory, but some were excitatory. 4. CC interneurons were divided into three classes on the basis of reticulospinal Müller cell inputs. CC1 interneurons were excited by the ipsilateral Müller cell B1 and the contralateral Mauthner cell. CC1 interneurons were inhibitory. They were excited polysynaptically by ipsilateral sensory dorsal cells and were inhibited by contralateral dorsal cells. They were distinguished morphologically by having no rostral axon branch and no contralateral dendrites. CC1 interneurons were phasically active during fictive swimming with their peak depolarizations preceding those of myotomal motoneurons by about 0.15 cycle. 5. CC2 interneurons were also inhibitory, but they were distinguished from CC1 interneurons by their excitation from the ipsilateral Müller cells B2-4 nd by their thin rostral and thicker caudal axonal branches on the contralateral side of the spinal cord. 6. CC3 interneurons were excitatory, and they were inhibited by the ipsilateral Müller cell I1. CC3 interneurons could have contralateral dendrites and bifurcating axons, and they had lower average axonal conduction velocities than CC1 and CC2 interneurons. 7. Inhibitory CC interneurons may be important for motor coordination in the lamprey. Movements of the lamprey body during reflexes and swimming consist of contraction and relaxation of myotomal muscles on opposite sides of the body. By being coactive with ipsilateral myotomal motoneurons, inhibitory CC interneurons could contribute to the inhibition of contralateral motoneurons during these movements.

Neuronal Substrates for State-Dependent Changes in Coordination between Motoneuron Pools during Fictive Locomotion in the Lamprey Spinal Cord

“…Individual CC-E interneurons can show in-phase activity to the ipsilateral ventral root and, thus, with contralateral fMN (Buchanan, 1986). Together, these results strongly indicate that these commissural excitatory interneurons, first described by Buchanan (1982Buchanan ( , 1986, are responsible for activating fMNs during fictive locomotion.…”

“…The specificity of such excitatory contralateral inputs for fMNs is substantiated by the observation that at the same stimulation site and stimulation strength, mMNs of the same segment were found to receive IPSPs from commissural interneurons of the contralateral side (Alford and Grillner, 1991;Büschges et al, 2000). Buchanan (1982) first identified intersegmentally caudally projecting commissural interneurons that monosynaptically excite motoneurons in the lamprey spinal cord, termed CC-E interneurons. Individual CC-E interneurons can show in-phase activity to the ipsilateral ventral root and, thus, with contralateral fMN (Buchanan, 1986).…”

“…Grillner (2003, 2005) showed that pattern generation for swimming in the lamprey spinal cord results from a hemisegmental glutamatergic network that generates a fast rhythm driving ipsilateral motoneurons. This rhythmicity is then transformed into an alternating activity pattern between both sides of the spinal cord by crossed glycinergic inhibition, which is mediated by inhibitory commissural interneurons (Grillner and Wallén, 1980;Buchanan, 1982Buchanan, , 2001 (Fig. 9).…”

“…In the lamprey spinal cord excitatory commissural interneurons with long descending axons have been described [excitatory contralaterally and caudally projecting interneurons (CC-E)] (Buchanan, 1982). To investigate whether a direct monosynaptic connection from these CC-E interneurons might be responsible for driving fMNs, the axons of these long range interneurons were stimulated contralaterally.…”

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.…”