THE ONSET OF RESPONSE HABITUATION DURING THE GROWTH OF THE LATERAL GIANT-NEURON OF CRAYFISH

1. The postembryonic development of the crayfish LG tailflip command neuron's response to mechanosensory input was studied with standard electrophysiological techniques in animals between 1 and 12 cm long. 2. LG neurons are present in each abdominal hemisegment where they receive direct and indirect excitatory input from mechanosensory afferents. In both small and large crayfish, electrical stimulation of an abdominal ganglionic nerve containing those afferents evoked a compound excitatory postsynaptic potential (EPSP) with an early, reliable alpha component and a later, depression-prone beta wave. It is known that the alpha and beta components are produced by inputs from primary mechanosensory afferents and interneurons, respectively. 3. In crayfish <2 cm long, LG was excited by the alpha component. When superthreshold, the alpha component triggered a single spike; additional excitation provided by the later beta wave presumably was preempted by refractoriness following the a spike and by recurrent inhibition of LG excited by the spike. LG was excited reliably by the a component in response to repeated superthreshold stimulation. 4. In crayfish between 2 and 3 cm, LG was excited more readily by the beta wave than by the alpha component. LG's beta spike response habituated to repeated stimulation at 1 Hz, and the beta EPSP depressed whereas the alpha component was largely unchanged. The appearance of the cellular substrates of habituation correlates with the reported onset of behavioral habituation of the tailflip response. Higher stimulus levels brought the alpha EPSP to threshold. Repetitive stimulation at these levels reliably evoked LG spikes from the alpha EPSP. 5. In crayfish >8 cm, stimulation of a single ganglionic nerve failed to bring the alpha EPSP to threshold, whereas simultaneous strong stimulation of two ipsilateral ganglionic nerves could do so. In these animals, the alpha spike and EPSP habituated in response to stimulus repetition rates as low as 0.1 Hz. These results suggest that LG receives depression-prone, excitatory chemical synaptic inputs from primary afferents in addition to rectifying electrical inputs. 6. To account for the increased stimulus threshold of an alpha spike in larger crayfish, alpha and beta EPSP amplitudes and spike thresholds were compared in small and large crayfish. In small (1 to 2.6 cm) crayfish, alpha and beta EPSPs at the dendrite and initial axon segment were similar in amplitude (the ratios alpha/beta calculated for the two sites equal 0.78 and 0.72, respectively), and each experienced similar attenuation in passing between the two sites. In large (>9 cm) crayfish, dendritic EPSPs were also similar (alpha/beta ratio was 0.89), but alpha fell with respect to beta at the initial axon segment (alpha/beta ratio was 0.38). Attenuation between the dendrite and initial axon segment was twice as great for alpha as for beta EPSPs. alpha and beta spike thresholds were equal in small crayfish and in large crayfish, although the thresholds were higher in large crayfish. 7. We conclude that during the growth of LG, the alpha stimulus threshold increases more than the beta stimulus threshold because attenuation of the alpha component increases more than attenuation of the beta wave. The change in relative stimulus threshold unmasks the depression-prone, disynaptic afferent pathway to LG, which accounts for the onset of habituation of both LG's response and tailflip behavior as crayfish grow beyond 2 cm in length.