Does the Mauthner cell conform to the criteria of the command neuron concept?

Rock, Michael K.; Hackett, John T.; Brown, D.L.

doi:10.1016/0006-8993(81)90648-x

Cited by 52 publications

(22 citation statements)

References 14 publications

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“…These criteria are as follows: (i) preferred access to sensory input, (ii) appropriate firing during the motor program, (iii) ability to drive the motor program directly when stimulated at physiological rates, and (iv) necessity of its firing for sensory input to be able to elicit the motor program (2,13). Other examples of individual neurons that satisfy, or nearly satisfy, this full set of criteria include interneuron 1 in the cricket acoustic avoidance response (35), the lateral giant cell in the crayfish tail-flip response (36), and the Mauthner cell in the teleost fish and amphibian tail-flip responses (37). One difference between these examples and DRI is that in each of the other cases the neuron in question drives a brief, single-phase reflex response, quite unlike the rhythmic swim motor program considered here, which can last a full minute or more.…”

Section: Discussionmentioning

confidence: 99%

Single neuron control over a complex motor program.

Frost

Katz

1996

Proc. Natl. Acad. Sci. U.S.A.

104

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While there are many instances of single neurons that can drive rhythmic stimulus-elicited motor programs, such neurons have seldom been found to be necessary for motor program function. In the isolated central nervous system of the marine mollusc Tritonia diomedea, brief stimulation (1 sec) of a peripheral nerve activates an interneuronal central pattern generator that produces the longlasting (-30-60 sec) motor program underlying the animal's rhythmic escape swim. Here, we identify a single interneuron, DRI (for dorsal ramp interneuron), that (i) conveys the sensory information from this stimulus to the swim central pattern generator, (ii) elicits the swim motor program when driven with intracellular stimulation, and (iii) blocks the depolarizing "ramp" input to the central pattern generator, and consequently the motor program itself, when hyperpolarized during the nerve stimulus. Because most of the sensory information appears to be funneled through this one neuron as it enters the pattern generator, DRI presents a striking example of single neuron control over a complex motor circuit.Over 30 yr ago, Wiersma and Ikeda (1) introduced the term "command neuron" to describe single interneurons in the crayfish that could drive coordinated movements of the animal's swimmerets. In its most restricted form, a command neuron is currently defined as a single interneuron, situated between sensory neurons and the motor pattern-generating circuitry, whose activity is both necessary and sufficient for sensory activation of the motor program (2). Many cells have now been described that can drive stimulus-elicited motor programs (3-13), but only rarely have such neurons been shown to also be necessary for circuit operation. Instead, in most cases these neurons have been found to operate in parallel with other circuit elements that fill-in when the cell in question is removed from the network (7-13). These and other findings have given rise in recent years to the view that, in most systems, command properties are distributed across broad interneuronal networks, with single neurons having only minor roles. We here describe a newly found interneuron in the Tritonia escape swim neural circuit that fulfills the strict definition of a command neuron (see also Discussion). The properties of this neuron, the dorsal ramp interneuron (DRI), provide further support for the original idea that the command function can be highly localized within a circuit, in this case, by funneling sensory information to the swim central pattern generator (CPG) and thereby controlling whether or not the swim motor program will be activated.When the marine mollusc Tritonia diomedea encounters the tube feet of certain predatory sea stars, it responds with a vigorous rhythmic escape swim, consisting of a series of alternating ventral and dorsal whole-body flexions (14, 15). The neural circuit generating this behavior has been wellstudied and consists of identified populations of afferent neurons (16,17), CPG neurons (18-24), and efferent neuronsThe ...

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Section: Discussionmentioning

confidence: 99%

Single neuron control over a complex motor program.

Frost

Katz

1996

Proc. Natl. Acad. Sci. U.S.A.

104

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“…These include the crayfish lateral giant fi bers [Olson and Krasne, 1981], neuron Int-1 in the cricket [Nolen and Hoy, 1984] and the giant fibers of the fruit fly [Wyman et al, 1984], As with the comparable stud ies on the Mauthner system [Hackett and Faber, 1983a;Rock et al, 1981], there is no argument with the validity of the experi mental findings, but rather with the para digm used to produce explanations of the findings. However, because the CNE is a non-contingent theory, our analysis pre dicts that for every interpretation of a CNE command neuron, there will be counterclaims whenever the conditions are altered or new details are uncovered about the interconnections of the system.…”

Section: Discussionmentioning

confidence: 99%

Command and the Neural Causation of Behavior: A Theoretical Analysis of the Necessity and Sufficiency Paradigm; pp. 149–164

Eaton¹,

DiDomenico²

1985

Brain Behav Evol

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The command concept is the prevalent explanation for initiation of behavioral acts. We review the theory and methods used to show the existence of neurons mediating command function according to a major approach, which we call the Command Neuron Experiment (CNE). The CNE claims that command neurons are the cause of, or are necessary and sufficient for, the execution of behavioral acts. In the CNE, command function is unequivocally localized to a structure, the command neuron. However, findings from an archetypal command neuron, the Mauthner cell, produce anomalous interpretations in the context of this theory. This conflict is the cumulative result of faulty causal, operational and behavioral themes in the CNE. These themes readily lead to false-positive or false-negative conclusions when its operational procedures are applied. We conclude that this concept must be abandoned. In a companion paper we propose a re-formulation of command as a dynamic system property that is intermediate to neurophysiological and behavioral contexts and independent of methods, structures, or preconceived causal schemes.

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“…Thus, it may be concluded that the Mauthner cell spike is associated with the tail flip. Furthermore, the tail flips of these preparations appear to correspond to the first stage or 'C bend' of startle responses of unrestrained tadpoles that have been described for R. catesbeiana, R. tem poraria, and X.laevis [Rock et al, 1981;Will, 1991]. Along with evidence from the electrophysiological data [Rock et ah, 1981], the assumption of a Mauthner cell involvement in the startle responses of free swim ming tadpoles of these species is also supported by the fact that I have not been able to elicit similar startle responses in B. bufo and B. orientalis [unpubl.…”

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confidence: 64%

“…If the startle response sequence of R. catesbeiana, as shown in the study of Rock et al [ 1981, fig. 1 presentative for that species, then there might also be species-specific differences between the responses of R. catesbeiana and R. temporaria: In the former the initial body bend is of the C type, and the second turn seems to start at about 60-80 ms after the onset of the response; in the latter, because of the prolonged in itial bending, the second turn does not occur before 80-100 ms after the response onset.…”

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confidence: 99%

Amphibian Mauthner Cells (Part 2 of 2)

Will¹

1991

Brain Behav Evol

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Presently available data on anatomical, electrophysiological, and behavioral aspects of the Mauthner cell in amphibians are reviewed. Urodelian Mauthner cells appear morphologically distinct from those in anurans with respect to their abundant somatic dendrites, axon cap structures, lack of nodes of Ranvier, and size of axon collaterals. The presence of Mauthner cells does not seem to correlate with the presence of a tail or with an aquatic life-style in either larvae or adults, as they are also found in terrestrial adults, as well as in species without an aquatic larval stage. Electrophysiological data on Mauthner cell circuits are available for only two anuran species and indicate some interspecific differences. Special attention is given to a comparison of startle responses in larval and adult anurans and their possible relationship to Mauthner cell activities. Because of specific differences in Mauthner cell activities, as well as in startle response performance, it is argued that amongst the various ichthyopsid species Mauthner cells may have been adapted to modified functions due to the diverse morphoecological situations in which they are found.

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Does the Mauthner cell conform to the criteria of the command neuron concept?

Cited by 52 publications

References 14 publications

Single neuron control over a complex motor program.

Single neuron control over a complex motor program.

Command and the Neural Causation of Behavior: A Theoretical Analysis of the Necessity and Sufficiency Paradigm; pp. 149–164

Amphibian Mauthner Cells (Part 2 of 2)

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