In a spinal turtle, unilateral stimulation in the rostral scratch receptive field elicited rhythmic fictive rostral scratching in ipsilateral hindlimb motor neurons; contralateral hip motor activity was also rhythmic and out-of-phase with ipsilateral hip motor activity. When left and right rostral scratch receptive fields were stimulated simultaneously, bilateral rhythmic fictive rostral scratching was produced; left hindlimb scratching was out-of-phase with right hindlimb scratching. Thus, spinal circuits coordinate interlimb phase during bilateral fictive scratching. We examined the contributions of contralateral spinal circuitry to the normal pattern of right hindlimb fictive rostral scratching by removing the left halves of the D7 segment and the hindlimb enlargement (D8-S2 segments). After left- hemicord removal, stimulation in the right rostral scratch receptive field usually elicited a variation of rostral scratching with rhythmic right hip flexor activity and no right hip extensor activity; thus, right hip flexor rhythm generation does not require left hindlimb enlargement circuitry. Normal right hindlimb rostral scratching with rhythmic alternation between hip flexor and extensor activities was rarely observed; thus, contralateral spinal circuitry contributes to the production of normal ipsilateral fictive rostral scratching. After left-hemicord removal, stimulation in the left rostral scratch receptive field elicited rhythmic right hip extensor activity; thus, contralateral spinal circuitry can generate a hip extensor rhythm during ipsilateral rostral scratch receptive field stimulation. Our observations and those of Berkowitz and Stein (1994a,b) support the concept that an ipsilateral hindlimb's normal rostral scratch motor pattern is generated by a modular central pattern generator that is bilaterally distributed in the spinal cord.
Analyses of fictive scratching motor patterns in the spinal turtle with transverse hemisection provided support for the concept of bilateral shared spinal cord circuitry among neurons responsible for generating left- and right-side rostral, pocket, and caudal fictive scratching. Rhythmic bursts of hip flexor activity, the hip extensor deletion variation of fictive rostral scratching, were elicited by ipsilateral stimulation in the rostral scratch receptive field of a spinal turtle [transection at the segmental border between the second (D2) and third (D3) postcervical spinal segments] with a contralateral transverse hemisection one segment anterior to the hindlimb enlargement (at the D6-D7 segmental border). In addition, other sites were stimulated in this preparation: (1) contralateral sites in a rostral, pocket, or caudal scratch receptive field or (2) ipsilateral sites in a caudal scratch receptive field. A reconstructed fictive rostral scratch motor pattern of rhythmic alternation between hip flexor and hip extensor activation was produced by simultaneous stimulation of one site in the ipsilateral rostral scratch receptive field and another site in one of the other scratch receptive fields. This reconstructed rostral scratch motor pattern resembled the normal rostral scratch motor pattern produced by one-site rostral scratch stimulation of a spinal turtle (D2-D3 transection) with no additional transections. The observation of a reconstructed rostral scratch motor pattern produced by two-site stimulation in the spinal turtle with transverse hemisection supports the concept that hip extensor circuitry activated by stimulation of other scratch receptive fields is shared with circuitry activated by ipsilateral rostral scratch receptive field stimulation.
1. We demonstrated multisecond increases in the excitability of the rostral-scratch reflex in the turtle by electrically stimulating the shell at sites within the rostral-scratch receptive field. To examine the cellular mechanisms for these multisecond increases in scratch excitability, we recorded from single cutaneous afferents and sensory interneurons that responded to stimulation of the shell within the rostral-scratch receptive field. A single segment of the midbody spinal cord (D4, the 4th postcervical segment) was isolated in situ by transecting the spinal cord at the segment's anterior and posterior borders. The isolated segment was left attached to its peripheral nerve that innervates part of the rostral-scratch receptive field. A microsuction electrode (4-5 microns ID) was used to record extracellularly from the descending axons of cutaneous afferents and interneurons in the spinal white matter at the posterior end of the D4 segment. 2. The turtle shell is innervated by slowly and rapidly adapting cutaneous afferents. All cutaneous afferents responded to a single electrical stimulus to the shell with a single action potential. Maintained mechanical stimulation applied to the receptive field of some slowly adapting afferents produced several seconds of afterdischarge at stimulus offset. We refer to the cutaneous afferent afterdischarge caused by mechanical stimulation of the shell as "peripheral afterdischarge." 3. Within the D4 spinal segment there were some interneurons that responded to a brief mechanical stimulus within their receptive fields on the shell with short afterdischarge and others that responded with long afterdischarge. Short-afterdischarge interneurons responded to a single electrical pulse to a site in their receptive fields either with a brief train of action potentials or with a single action potential. Long-afterdischarge interneurons responded to a single electrical shell stimulus with up to 30 s of afterdischarge. Long-afterdischarge interneurons also exhibited strong temporal summation in response to a pair of electrical shell stimuli delivered up to several seconds apart. Because all cutaneous afferents responded to an electrical shell stimulus with a single action potential, we conclude that electrically evoked afterdischarge in interneurons was produced by neural mechanisms in the spinal cord; we refer to this type of afterdischarge as "central afterdischarge." 4. These results demonstrate that neural mechanisms for long-lasting excitability changes in response to cutaneous stimulation reside in a single segment of the spinal cord. Cutaneous interneurons with long afterdischarge may serve as cellular loci for multise
1. A low-spinal, immobilized turtle displays a fictive scratch reflex in hindlimb motor neurons in response to tactile stimulation of the shell (17, 19). Turtles exhibit three forms of the scratch reflex: rostral, pocket, and caudal. Each form is elicited by tactile stimulation of a different receptive field on the body surface. The ventral-posterior pocket (VPP) cutaneous nerve innervates the ventral-posterior portion of the pocket scratch receptive field (Fig. 1). Natural stimulation within the VPP nerve's receptive field evoked a pocket scratch reflex (Fig. 2A). Electrical stimulation of this nerve elicited robust pocket scratch reflexes (Fig. 2, B and C). 2. A single electrical pulse to the VPP nerve delivered at a voltage (greater than 5 V, 0.1 ms) that activated all the axons in the nerve was termed a "maximal" pulse. A single maximal pulse did not evoke a scratch motor response. It raised the excitability of the pocket scratch central pattern generator for several seconds, however. We revealed such excitability changes by applying maximal pulses to the VPP nerve at multisecond intervals (Figs. 5 and 6). When we delivered maximal pulses with interpulse intervals of less than or equal to 5 s, the first pulse produced no motor response and the second pulse evoked one or more cycles of pocket scratch. 3. A stimulus pulse applied to the VPP nerve was used as a probe for studying changes in the excitability of the pocket scratch CPG following scratch motor patterns. In a rested preparation, the stimulus pulse did not activate motor output. In contrast, the stimulus pulse evoked one or two cycles of pocket scratch activity if delivered within 2.5 s after the cessation of rhythmic pocket scratch motor activity (Figs. 7-9). These results are consistent with the hypothesis that the pocket scratch CPG has elevated excitability for seconds following the cessation of pocket scratch motor output. A single pulse applied to the VPP nerve evoked no response if delivered after the cessation of rostral scratch motor activity, however (Fig. 9D). 4. We used a train of maximal pulses to the VPP nerve to probe the form-specificity of the changes in the excitability following a rostral scratch motor pattern (Fig. 10). We set the stimulus parameters so that the train evoked one or two cycles of a pocket scratch motor pattern in a preparation that had rested for over 1 min.(ABSTRACT TRUNCATED AT 400 WORDS)
Fictive swimming was elicited in low-spinal immobilized turtles by electrically stimulating the contralateral dorsolateral funiculus (cDLF) at the level of the third postcervical segment (D(3)). Fictive hindlimb motor output was recorded as electroneurograms (ENGs) from up to five peripheral nerves on the right side, including three knee extensors (KE; iliotibialis [IT]-KE, ambiens [AM]-KE, and femorotibialis [FT]-KE), a hip flexor (HF), and a hip extensor (HE). Quantitative analyses of burst amplitude, duty cycle and phase were used to demonstrate the close similarity of these cDLF-evoked fictive motor patterns with previous myographic recordings obtained from the corresponding hindlimb muscles during actual swimming. Fictive rostral scratching was elicited in the same animals by cutaneous stimulation of the shell bridge, anterior to the hindlimb. Fictive swim and rostral scratch motor patterns displayed similar phasing in hip and knee motor pools but differed in the relative amplitudes and durations of ENG bursts. Both motor patterns exhibited alternating HF and HE discharge, with monoarticular knee extensor (FT-KE) discharge during the late HF phase. The two motor patterns differed principally in the relative amplitudes and durations of HF and HE bursts. Swim cycles were dominated by large-amplitude, long-duration HE bursts, whereas rostral scratch cycles were dominated by large-amplitude, long-duration HF discharge. Small but significant differences were also observed during the two behaviors in the onset phase of biarticular knee extensor bursts (IT-KE and AM-KE) within each hip cycle. Finally, interactions between swim and scratch motor networks were investigated. Brief activation of the rostral scratch during an ongoing fictive swim episode could insert one or more scratch cycles into the swim motor pattern and permanently reset the burst rhythm. Similarly, brief swim stimulation could interrupt and reset an ongoing fictive rostral scratch. This shows that there are strong central interactions between swim and scratch neural networks and suggests that they may share key neural elements.
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