Conditioned modification of phototactic behavior in Hermissenda. II. Differential adaptation of B-photoreceptors

Abstract

Changes in the response of B-type photoreceptors to illumination were examined in the isolated nervous systems of Hermissenda following the conditioning procedures described in the preceding paper. Analysis of the transient peak amplitude of the depolarizing generator potential at the onset of two of the three light intensities used in the behavioral studies did not reveal an enhanced photoresponse to the light. However, when the activity of the same B-photoreceptors was examined after 5 min of continuous light, there was a significant decrease in the light-adapted discharge rate and a decreased generator potential amplitude in conditioned animals as compared to the random controls. An examination of the light adapted photoresponse in preparations where spike generation and synaptic interactions were eliminated showed that the decreased photoresponse of conditioned animals was due to factors that are intrinsic to the B-photoreceptors. These results are consistent with previous work suggesting that conditioning produces substantial adaptation effects in B-photoreceptors (Crow, T. (1982) Soc. Neurosci. Abstr. 8: 824). Since the cellular changes qualitatively follow the behavioral changes and are observed at times and light intensities that are similar to those where the suppression of phototactic behavior is expressed, phototactic suppression may be directly related to the changes in the B-photoreceptors and may not require the previously proposed complex network interactions within the eyes of Hermissenda.

Synaptic Enhancement and Enhanced Excitability in Presynaptic and Postsynaptic Neurons in the Conditioned Stimulus Pathway ofHermissenda

“…The ratio is expressed as A/(A ϩ B), where A represents pretraining scores and B represents post-training scores. Conditioned animals exhibited behavioral suppression that was similar in magnitude to previous reports (Crow and Alkon, 1978;Crow and Offenbach, 1983;Crow, 1985). After postaquisition testing, all animals were coded so that the collection of electrophysiological data was conducted using blind experimental procedures.…”

“…The details of the conditioning procedures and methods for testing phototactic behavior have been described previously in detail (Crow and Alkon, 1978;Crow and Offenbach, 1983;Crow, 1985) and will be described only briefly in this report. Animals were tested before training to determine baseline latencies to initiate locomotion in response to a test light.…”

“…In conditioned Hermissenda, enhanced excitability and synaptic enhancement have been identified as cellular correlates of associative learning in the pathway supporting the conditioned stimulus (CS) (Crow and Alkon, 1980;Farley and Alkon, 1982;Alkon et al, 1985;Crow, 1993, 1994). Enhanced excitability in identified neurons of conditioned Hermissenda is expressed by increases in spike frequency elicited by extrinsic current, an increase in the input resistance of type B photoreceptors, decreased spike frequency accommodation, an alteration in the amplitude of light-induced generator potentials, and a decrease in several K ϩ conductances (Crow and Alkon, 1980;Alkon et al, 1982Alkon et al, , 1985Farley and Alkon, 1982;West et al, 1982;Crow, 1985;Farley et al, 1990;Frysztak and Crow, 1993). In addition to the nonsynaptic enhancement in excitability detected after conditioning, enhancement of the amplitude of monosynaptic IPSPs has been observed in conditioned Hermissenda (Frysztak and Crow, 1994).…”

Inhibition of Conditioned Stimulus Pathway Phosphoprotein 24 Expression Blocks the Reduction in A-Type Transient K+Current Produced by One-TrialIn VitroConditioning ofHermissenda

“…Previous studies of associative learning in Hermissenda have shown that pavlovian conditioning results in long-term intrinsic enhanced excitability of neurons in the CS pathway (Crow and Alkon, 1980;Farley and Alkon, 1982;West et al, 1982;Crow, 1985;. Voltage-clamp studies identified a reduction in several K ϩ currents, I A and I K,Ca , as contributors to conditioning-dependent enhanced excitability (Alkon et al, Ϫ1 , where V 1/2 is the half-activation voltage, and k m is the maximum slope.…”

“…In Hermissenda, one site of intrinsic excitability changes produced by pavlovian conditioning is neurons in the conditioned stimulus (CS) pathway (Crow and Alkon, 1980;Farley and Alkon, 1982;Alkon et al, 1985;Crow, 1985Crow, , 1988Goh et al, 1985;Matzel et al, 1990;Frysztak and Crow, 1993, 1997Gandhi and Matzel, 2000;. In animals that exhibit intrinsic enhanced excitability, a cytoskeletal-related protein, the phosphorylation of which is regulated by conditioning, has been identified in components of the CS pathway Xue-Bian, 2000, 2002).…”