Both shared and specialized spinal circuitry for scratching and swimming in turtles

Berkowitz, Ari

doi:10.1007/s00359-002-0297-7

Cited by 62 publications

(104 citation statements)

References 54 publications

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“…Examination of both extracellular and intracellular recordings in turtle fictive and nonfictive preparations by Stein, Berkowitz, Currie, Hounsgaard, and others also show both shared and dedicated neurons recruited in fictive vertebrate motor patterns (Berkowitz, 2001(Berkowitz, , 2002(Berkowitz, , 2008Alaburda et al, 2005;Stein, 2005Stein, , 2008Berg et al, 2007;Samara and Currie, 2008). However, their data cannot or did not examine modularity in terms of premotor drive, or examine EMG and force patterns as we did here.…”

Section: Spinal Interneuron Systems and Recordings In Other Lower Tetmentioning

confidence: 50%

A Neural Basis for Motor Primitives in the Spinal Cord

Hart

Giszter²

2010

J. Neurosci.

244

194

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Motor primitives and modularity may be important in biological movement control. However, their neural basis is not understood. To investigate this, we recorded 302 neurons, making multielectrode recordings in the spinal cord gray of spinalized frogs, at 400, 800, and 1200 m depth, at the L2/L3 segment border. Simultaneous muscle activity recordings were used with independent components analysis to infer premotor drive patterns. Neurons were divided into groups based on motor pattern modulation and sensory responses, depth recorded, and behavior. The 187 motor pattern modulated neurons recorded comprised 14 cutaneous neurons and 28 proprioceptive neurons at 400 m in the dorsal horn, 131 intermediate zone interneurons from ϳ800 m depth without sensory responses, and 14 motoneuron-like neurons at ϳ1200 m. We examined all such neurons during spinal behaviors. Mutual information measures showed that cutaneous neurons and intermediate zone neurons were related better to premotor drives than to individual muscle activity. In contrast, proprioceptive-related neurons and ventral horn neurons divided evenly. For 46 of the intermediate zone interneurons, we found significant postspike facilitation effects on muscle responses using spike-triggered averages representing short-latency postspike facilitations to multiple motor pools. Furthermore, these postspike facilitations matched significantly in both their patterns and strengths with the weighting parameters of individual primitives extracted statistically, although both were initially obtained without reference to one another. Our data show that sets of dedicated interneurons may organize individual spinal primitives. These may be a key to understanding motor development, motor learning, recovery after CNS injury, and evolution of motor behaviors.

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Section: Spinal Interneuron Systems and Recordings In Other Lower Tetmentioning

confidence: 50%

A Neural Basis for Motor Primitives in the Spinal Cord

Hart

Giszter²

2010

J. Neurosci.

244

194

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“…Fictive hindlimb scratching was elicited by gentle rubbing of the shell or skin with the glass probe. Fictive swimming was evoked using a pair of 100 m silver wires to deliver a 40 Hz train of bipolar electrical stimuli to the left D3 lateral funiculus (Lennard and Stein, 1977;Juranek and Currie, 2000;Berkowitz, 2002). All signals were stored using a digital audio tape recorder (TEAC America, Montebello, CA) and analyzed off-line using Datapac 2000 software (Run Technologies, Laguna Hills, CA).…”

Section: Methodsmentioning

confidence: 99%

“…It is now known, for example, that many, but not all, of the spinal premotor interneurons that contribute to fictive struggling also contribute to fictive swimming in embryonic tadpoles (Soffe, 1993). Similarly, many but not all of the spinal interneurons that contribute to fictive scratching are also activated during fictive swimming in turtles (Berkowitz, 2002(Berkowitz, , 2005.…”

Section: Introductionmentioning

confidence: 99%

Spinal Interneurons That Are Selectively Activated during Fictive Flexion Reflex

Berkowitz¹

2007

J. Neurosci.

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Behavioral choices in invertebrates are mediated by a combination of shared and specialized circuitry, including neurons that are inhibited during competing behaviors. Less is known, however, about the neural mechanisms of behavioral choice in vertebrates. The spinal cord can appropriately select among several types of limb movements, including limb withdrawal (flexion reflex), scratching, and locomotion, and thus is conducive to examination of vertebrate mechanisms of behavioral choice. Flexion reflex can interrupt and reset the rhythm of scratching and locomotion, suggesting that a combination of shared and specialized circuitry contributes to these behaviors, but little is known about the interneurons involved. Here, I used in vivo intracellular recording and dye injection to identify a group of spinal interneurons that are strongly activated during fictive flexion reflex but inhibited during fictive scratching and fictive swimming. These flexion-selective interneurons are typically rhythmically hyperpolarized during fictive scratching and fictive swimming. This hyperpolarization can be maximal during the ipsilateral hip flexor bursts of rhythmic limb motor patterns, although these cells are strongly activated during the ipsilateral hip flexor bursts of fictive flexion reflex. Thus, these interneurons are relatively specialized for fictive limb withdrawal, rather than contributing to the hip flexor phase of multiple types of limb movements. These flexion-selective cells are physiologically and morphologically distinguishable from a recently described group of spinal interneurons (transverse interneurons) that are strongly activated during both fictive flexion reflex and fictive scratching. Thus, spinal interneurons with distinct behavioral roles may to some extent be morphologically distinguishable.

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“…In this respect, scratching in limbed vertebrates is an exception because the entire sensorimotor transduction is executed by a network of neurons confined to a few spinal segments without the need of other parts of the CNS (Gelfand et al, 1988;Stein, 2005). Scratching has been studied in detail in the cat (Orlovsky et al, 1999) and the turtle in vivo (Robertson and Stein, 1988;Currie and Gonsalves, 1999;Berkowitz, 2001Berkowitz, , 2002Berkowitz, , 2005Stein, 2005;Samara and Currie, 2008) but crucially, the spinal cord of the adult turtle is also uniquely amenable to experimentation in vitro (Keifer and Stein, 1983;Hounsgaard and Nicholson, 1990;Currie and Lee, 1996;Alaburda and Hounsgaard, 2003). In vitro experiments provide data of sufficient detail to make mathematical analysis of cell properties and synaptic network activity meaningful (Booth et al, 1997;Svirskis et al, 2000Svirskis et al, , 2001Svirskis and Hounsgaard, 2003;Berg et al, 2008).…”

Section: Introductionmentioning

confidence: 99%