Robert N. Leaton

Potentiated Startle: Its Relation to Freezing and Shock Intensity in Rats

Acoustic startle response and freezing were measured in a potentiated startle paradigm in which a startle stimulus was presented either alone or in the presence of a light conditioned stimulus (CS) which had been paired previously with either 1-mA or 3-mA footshock. During the CS the 1-mA group had higher startle amplitudes and a higher percentage of freezing than the 3-mA group. Startle amplitude was positively correlated with freezing under all conditions. The nonmonotonic relation between potentiated startle and shock intensity replicated Davis and Astrachans (1978) study. However, rather than suppressing startle, as they suggested, freezing facilitated startle and, like startle amplitude, was nonmonotonically related to shock intensity. Experiment 2 replicated these results and showed a regularly decreasing monotonic extinction function for potentiated startle and shock-associated freezing for both shock-level groups. Brown, Kalish, and Farber (1951) reported that the magnitude of the acoustic startle response was increased when the startle-eliciting stimulus was presented in conjunction with a stimulus previously paired with shock. This phenomenon, now commonly called the potentiated startle effect, has been frequently

Lesions of the cerebellar vermis and cerebellar hemispheres : effects on heart rate conditioning in rats

The effects of lesions of the cerebellum on the acquisition of heart rate (HR) conditioned responses (CRs) were examined in rats. Large lesions of the cerebellar vermis severely attenuated the acquisition of differentially conditioned bradycardic responses in restrained rats without affecting unconditioned HR responses to the tone conditioned stimuli (CSs) or the shock unconditioned stimulus (UCS). In a second experiment, rats were trained unrestrained, and under these conditions the CR was tachycardia in control animals. Lesions of the vermis again severely attenuated acquisition of this CR without affecting unconditioned responses to the CSs or UCS. Bilateral lesions of the cerebellar hemispheres did not affect HR conditioning in either test procedure. It is concluded that the vermis of the cerebellum is an essential component of an HR conditioning circuit in the rat. The cerebellar hemispheres, which are critically involved in some discrete somatomotor CRs, apparently have no essential functional contribution to HR conditioning. The results of these experiments implicating the midline cerebellar vermis in autonomic conditioning are discussed in relation to contributions from a forebrain system involved in HR conditioning and in relation to lateral cerebellar contributions to discrete somatomotor CRs.

Effects of cerebellar vermal lesions on species-specific fear responses, neophobia, and taste-aversion learning in rats

The cerebellar vermis has extensive anatomical connections with many brain stem and forebrain structures which have been implicated in emotional or affective behavior. Previous reports indicate that lesions of the vermis in a variety of experimental animals result in altered emotional behavior. The studies reported here attempted to clarify the nature of the change in emotional behavior following vermal lesions in rats by testing the animals in a variety of fear-eliciting situations. As compared with controls, vermal-lesioned rats froze less in the presence of a cat and showed fewer signs of fear in an open field. However, their responses to footshock did not differ fundamentally from controls. They recovered more quickly than controls from the neophobic response to a novel taste but showed robust taste-aversion learning. The results are discussed in terms of the role of the cerebellum in the modulation of fear-related behaviors and in terms of similarities and differences with the effects of amygdala lesions. The results expand the body of data implicating the cerebellum in the modulation of complex motivational behavior.

Influence of Long-Term Sensitization on Long-Term Habituation of the Acoustic Startle Response in Rats: Central Gray Lesions, Preexposure, and Extinction

The relation between long-term decrements of the acoustic startle response in rats and the development of freezing behavior during habituation training was examined. Freezing behavior developed over the initial trials of habituation training, and the rate of long-term response decrements was found to be inversely related to the development of freezing. Manipulations (neurological or behavioral) that either reduced the level of freezing or retarded its development promoted startle response decrements. In Experiment 1, rats receiving electrolytic lesions of the ventrolateral periaqueductal gray demonstrated both accelerated long-term startle response decrements and retarded development of freezing behavior. In Experiment 2, preexposure to the startle apparatus (i.e., latent inhibition) accelerated long-term startle decrements and inhibited development of freezing. In Experiment 3, exposure to the startle apparatus following initial habituation training (i.e., extinction) reduced both freezing behavior and startle response amplitudes. The results are discussed in terms of the influence of Pavlovian fear conditioning on long-term habituation of the acoustic startle response.

Potentiation of the Acoustic Startle Response by a Conditioned Stimulus Paired With Acoustic Startle Stimulus in Rats

The hypothesis that the standard acoustic startle habituation paradigm contains the elements of Pavlovian fear conditioning was tested. In a potentiated startle response paradigm, a startle stimulus and a light conditioned stimulus (CS) were paired. A startle stimulus then was tested alone or following the CS. Freezing behavior was measured to index conditioned fear. The startle response was potentiated on CS trials, and rats froze more in CS than in non-CS periods. In Experiment 1, response to a previously habituated, weak startle stimulus was potentiated. In Experiment 2, response to the same stimulus used as the unconditioned stimulus (US) in training was potentiated. This CS-potentiated response retarded the course of response decrements over training sessions as compared with an explictly unpaired control group. Conditioned fear is a standard feature of this habituation paradigm, serves to potentiate the startle response, and provides an associative dimension lacking in the habituation process per se.

Cerebellar vermis: essential for classically conditioned bradycardia in the rat

The effects of lesions of the cerebellar vermis on the acquisition of heart-rate conditioning in rats was examined. Lesions of the vermis severely attenuated the acquisition of conditioned bradycardic responses in a simple conditioning procedure in restrained rats. Importantly, the vermal lesions did not affect resting heart-rate, unconditioned heart-rate orienting responses to a tone stimulus or unconditioned heart-rate responses to the shock unconditioned stimulus. It is concluded that the cerebellar vermis is an essential component of a heart-rate conditioned response circuit in the rat. The similarities between these effects and those following manipulations of the amygdala are discussed.

Medial Cerebellum and Long-Term Habituation of Acoustic Startle in Rats

Three experiments assessed the effects of damage to the medial cerebellum on long-term habituation (LTH) of the acoustic startle response. Experiment 1 replicated previous results. Lesions of the cerebellar vermis blocked LTH without affecting initial response levels or short-term habituation (STH). The lesions did not disrupt LTH of a simultaneously measured lick-suppression response. In Experiment 2, vermal lesions again blocked LTH of acoustic startle. Control lesions of the cerebellar hemispheres did not affect LTH. In Experiment 3, lesions to the medial (fastigial) cerebellar nuclei blocked LTH. Lesions to the lateral (dentate and interpositus) nuclei did not affect LTH. It is concluded that the medial cerebellum (cortex and nuclei) is part of the essential circuitry for LTH of acoustic startle, whereas the lateral cerebellum is not involved in the basic habituation process.

Habituation of the acoustic startle response in rats after lesions in the mesencephalic reticular formation or in the inferior colliculus.

Extensive damage to the mesencephalic reticular formation (MRF) in rats altered long-term habituation of the acoustic startle response without disrupting short-term habituation. The MRF lesions did not alter initial startle amplitudes, but the animals with lesions were unable to attain as low a long-term asymptote of habituation as could control animals. Subsequent manipulation of stimulus intensity and interstimulus interval revealed no differences in short-term habituation between the two groups. Large lesions to the inferior colliculus (IC) did not disrupt long-term habituation of the acoustic startle response, but these animals were unable to suppress responding as much as controls to intense stimuli presented rapidly. The deficits in long-term habituation following MRF lesions suggested a disruption of an extrinsic, inhibitory mechanism of habituation. The deficits following IC lesions could be due either to a disruption of a short-term habituation mechanism or to an increase in response sensitization produced by the lesions.

The effect of amygdala lesions on conditional and unconditional vocalizations in rats

Electrolytic lesions centered on the amygdaloid central nucleus (ACe) resulted in the inability of rats to acquire a Pavlovian conditional vocalization response. Conditioning consisted of pairing a light conditional stimulus with a tailshock unconditional stimulus (US). The thresholds of three unconditional responses (URs) to tailshock were assessed prior to conditioning. These URs are organized at spinal (spinal motor reflexes), medullary (vocalizations during shock), and forebrain (vocalization afterdischarges, VADs) levels of the neuraxis. Compared to sham-lesioned controls, rats with amygdala lesions exhibited a selective elevation in the threshold of VADs. During conditioning the amplitude and duration of VADs were selectively reduced in amygdala-lesioned rats. These findings support earlier observations of that elicitation of VADs by tailshock correlates with the capacity of this US to support fear conditioning. The ACe may be involved in both associative and non-associative aspects of fear conditioning, but for progress in our understanding it is essential to evaluate its role in the generation of conditioning relevant URs.

Locomotor activity, auditory startle and shock thresholds in spontaneously hypertensive rats ☆

A group of SHRs and a group of WKY normotensive controls were compared sequentially on open-field behavior, Y-maze activity, responsiveness and habituation of the auditory startle response, and shock thresholds. In the open field and Y maze the SHRs were more active than the WKYs, but the locomotor activity of the SHRs decreased more within sessions. However, the SHRs could be described as showing more, less or the same between-session habituation depending upon the apparatus and the portion of the session analyzed. The SHRs were less responsive than controls on the auditory startle response measure, and they did not differ from controls on startle-response habituation. The SHRs were less responsive than controls at low shock levels but more responsive at high shock levels. The relationship between SHRs and WKYs on the responsiveness dimension depended upon the modality and intensity of the stimulus, the response characteristics of the test situation, and the time sample of behavior taken.