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Crayfish Escape Behavior and Central Synapses. II. Physiological Mechanisms Underlying Behavioral Habituation

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Crayfish Escape Behavior and Central Synapses. II. Physiological Mechanisms Underlying Behavioral Habituation Crayfish Escape Behavior and Central Synapses. II. Physiological Mechanisms Underlying Behavioral Habituation ROBERT S. ZUCKER Department of Biological Sciences and Program in the Neurological Sciences, Stanford Unillersity, Stanford, California 94305 THE PREVIOUS PAPER (58) OLlth’led thC. CirCUit 33, 36), so the labilities in the circuit effer- responsible for exciting the lateral giant ent from the lateral giant cannot contribute neuron and initiating single tail flips in importantly to habituation of escape be- response to phasic mechanical stimuli to the havior. tail of crayfish. It was shown that the exci- In this paper, various possible sources of tation of some tactile interneurons by tac- lability in the afferent limb of the circuit tile afferents antifacilitates extensively at are explored. It appears that only presynap- low repetition rates. This phenomenon tic depression in the afferent to interneuron must be presumed to contribute to the synapse can account for the habituation. habituation of the response. It is not clear, Furthermore, there is a quantitative corre- however, that this is the only phenomenon spondence between the properties of the in- responsible for generating lability in the terneuronal excitatory postsynaptic poten- behavior. Receptor fatigue, variable proper- tial (EPSP), the nature of the circuit, and ties of the excitable membranes of the lat- the properties of the behavior. eral giant or the tactile interneurons, or labile properties of the circuit efferent to METHODS the giant are additional possibilities. One other point of lability has in fact been Crayfish (Procambarus clarkii) were main- tained and prepared for experiments as de- found. The strength of transmission at the scribed in the previous paper (58). The abdo- neuromuscular junction between the motor men was pinned ventral side up in cold saline, giant neuron and the phasic flexor muscles and the nerve cord was exposed and illumi- is very sensitive to stimuli recurring only nated with transmitted light. Single axons of once per minute; this junction rapidly interneurons were dissected from the nerve cord ceases to transmit activity after only a few for stimulation and recording with suction elec- stimuli (6). The motor giant is sometimes trodes, and their activity was monitored by a excited by the lateral giant (20, 39), and so suction electrode placed on the nerve cord. The it appears that this is a source of declining afferent activity was monitored with suction response strength in the efferent limb of electrodes placed on ganglionic roots. Stimuli were applied by brushing tactile hairs on the the neural circuit mediating escape. How- carapace or shocking an afferent root through an ever, this loss of transmission is adequately additional suction electrode. Microelectrode re- compensated by the continued activation of cordings were made from the ventrolateral den- several nongiant flexor motoneurons, whose drites of the lateral giant or the axons of inter- neuromuscular junctions facilitate (33, 39). neurons near their dendritic trees, using the Furthermore, electrical stimulation of the procedures described in the previous paper. lateral giant axon at frequencies up to 5 Hz The stimulating and recording apparatus was can elicit up to 50 apparently normal tail as described earlier. flips (unpublished observations; see also ref For experiments with single tactile receptors, the animals were prepared differently (31). The Received for publication August 30, 1971. nerve roots to all but the last abdominal gan- 621 622 It. S. ZtJCKER t$011 wc:rc sc\‘erc(l, and the tclsotr and uropotls, together with the sixth ganglion and the nerve cord, were separated from the abdomen, and pinnetl dorsal side up onto a Sylgard (Dow Corning Coq>., Micllnnd, Micll.) block in the preparation cllamber. Tactile hairs were excited by mech;uiical pulses generated by a piezoelec- tric “cutter” crystal (Brush Development Co., Cleveland, Ohio), driven by I-msec square pulses, provided by a Tektronix pulse generator. Aff eren t discharges were recorded from the fourth root with a suction electrode, and displayed and photographed conventionally. Successive-interval plots, used to represent adap- tation, were computed manually using measure- ments from the film. RESULTS Physiological fwoccsses responsible foj hehauio~al habituation RECEPTOR FATIGUE. The first possible source of response lability in a reflex arc lies in the response properties of the recep- tor cells. An initial attempt at determining their response characteristics to repeated sensory stimulation is illustrated in Fig. 1. FIG. 1. Tactile afferents do not fatigue to re- In five crayfish, the responses of tactile af- peated phasic stimulation. Twelve air bubbles were ferents were monitored in a second root, the made to strike pleural plate hairs at 0.5 Hz, while responses of tactile interneurons were re- recording the habituating responses of the lateral corded in the nerve cord, and the intracel- giant intracellularly in the third abodminal segment (top trace in A) and the activity of tactile inter- lular depolarization in the lateral giant was neurons in the nerve cord in the Z/3 connective observed, to repeated phasic tactile s timula- (bottom trace in A). The afferent volley (middle tion. I’he stimuli were provided by air trace) remains constant to repeated stimulation. bubbles blown from a pipette to strike A, andA illustrate the first and ninth responses, against a pleural plate once every 2 sec. The rcspcctively; B shows the amplitude of the lateral giant EPSP and the total number of afferent and average strength of the afferent volley re- in terneuron discharges to each stimulus. mained constant, while the responses in the giant cell and interneurons waned. It ap- pears that the receptors report the constant- teristics of one or both of the afferent in tensi ty stimulus faith fully. neurons were determined. Adaptation was It might be argued that fatigue is actually measured by lowering the stimulator probe occurring in small afferents whose spikes onto a tactile hair for a few seconds, while cannot be distinguished in peripheral root monitoring the afferent activity in the recordings. To meet this objection, the fourth root. The response was characteristic properties of a representative population of for each afferent, and their properties fell tactile hairs known to excite the lateral along a continuum between rather tonically giant mono- and polysynaptically were in- responding cells to very phasic cells which vestigated in five animals. A readily acces- fired a burst only at the beginning of the sible population of such hairs occurs on the stimulus (Fig. 2). All receptors studied, re- dorsal surface of the telson (3 1, SO). Using gardless of their adapting tendencies, showed a semi-isolated nerve cord (see METHODS), constant response magnitudes or response single dually innervated hairs (3, 43) were probabilities to phasic mechanical stimuli excited tonically or phasically with a me- repeated at 0.5 Hz. No receptors could be chanical vibrator, and the response charac- found that displayed any significant fatigue BASIS OF HABITUATION 623 I Successive, blochs OC CivQ ktimuli 400 0 300 0 ‘200 - O 100 I ooo I 11 3000 On s) FIG. 2. Propel-tics of single tactile hairs on the t&on, known to excite tactile interncuron A chemically and the lateral giant electrically (60). For each of three hairs, 25 phasic stimuli were applied at -05 Hz and the number of impulses to successive groups of five stimuli arc plotted in the top row. This is a measure of fatigue; each hair shows a constant level of excitability. In the bottom row are shown responses of the same hairs to tonic stimuli lasting for the length of the abscissa. Successive spike intervals (inverse frequency) are plotted on the ordinate as a function of the latency of each spike from the stimulus on the abscissa. This is a measure of adaptation. A shows a hair responding very phasically to a stimulus lasting 3 set; B presents a receptor with prominent phasic and tonic phases to its response; Ivhile the hair in C responds more tonically to a maintained stimulus. in response to this stimulus. On the other resulting from impulse firing, which may be hand, similar stimuli repeatedly delivered relative, prolonged, and accumulating (17, to tactile receptors invariably elicit a rapidly 19, 28, 55); and 2) prolonged accommoda- habituating escape response. It is concluded tion or adaptation, brought about by per- that receptor fatigue does not contribute sistence of the stimulus (10, 16, 48). significantly to habituation of this behavior. T-I wo-- tests were- --_~- made for accommodation This conclusion is consistent with the result in the lateral giant. The experiments were that habituation can be elicited just as easily specifically designed to reveal neural phe- by peripheral root stimulation as by phasic nomena with properties which might con- mechanical stimulation. tribute to behavioral habituation. If the lateral giant becomes lessexcitable as a con- ACCOMMODATION AND REFRACTORINESS IN LAT- sequence of being subjected to repeated ex- ERAL GIANT NEUKON. The process of excita- citatory depolarization, then its threshold tion of spikes in active membranes involves should increase after a series of stimuli several time-dependent phenomena which which cause habituation. Figure 3 illustrates can contribute to a lability in the process. one of five experiments in which a micro- Most changes in the responsiveness, excita- electrode in the lateral
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