Research reportBrief light as a practical aversive stimulus for the albino rat
Introduction
Electric footshock has served as the prototypical aversive stimulus in experimental preparations using rats [34], [30]. Footshock is popular for its reliability, utility at a wide range of current, and the feasibility of titrating shock levels for individual subjects. But electric shock has its downsides: It often induces secondary effects such as long-term sleep disruption [41], altered social behavior [27], reduction in locomotion, rearing, and grooming behaviors, as well as an increase in immobility and defecation [44]. Footshock has also received criticism when used to model conditions such as depression or anxiety disorder that are produced by stressors that lack a comparable component of pain [28]. Finally, the nature of footshock stimulation precludes its full inclusion in some modern experimental techniques, such as electrophysiology.
As neural, behavioral, and genetic research strives to create better animal models of human disorders, the availability of options other than footshock as aversive stimuli becomes increasingly important. Reed and Yoshino [39] recently noted the utility of a broader range of aversive stimuli, including some that might replace shock and avoid some of the drawbacks that accompany its use. For instance, they demonstrated that response suppression could be effected by a loud, short tone presented with long inter-trial intervals.
The present study aims to systematically test whether bright light is an effective aversive stimulus for rats. Early experiments demonstrated that rats will press a lever to terminate a light stimulus, and that rate of lever pressing increases with light intensity [19]. The rate of escape lever presses is also sensitive to the schedule of negative reinforcement [16], [17], [18]. When allowed to control their own daily exposure to light by lever pressing, albino rats decrease their exposure to light intensities greater than 1.25 lux over days, and maintain their exposure to light below this threshold [22], [23], [24], [25]. Further examination led Campbell and Messing [6] to suggest that light is likely aversive even at the lowest levels of illumination in rats. However, a considerable number of studies have proposed that light – at some levels – may not be aversive [36], and might even act as a reinforcer [2], [14], [40].
The following experiments provide a systematic test of light's efficacy as an aversive stimulus. Experiment 1 examined the aversiveness of bright light in a choice situation by adding a light contingency onto one of two otherwise identical alternatives. Experiments 2 and 3 examined escape from and avoidance of light, respectively. It has long been suggested that defensive responses are more efficiently learned when they are consistent with the natural repertoire of the animal [4]. Burrowing is a commonly observed defensive behavior in Rattus norvegicus [3], [20], [33], [35]. It was thus expected that entering a short tunnel would be an effective escape/avoidance response to light.
Section snippets
Experiment 1: punishment
It has been shown that rats prefer dark or dim areas over those that are brightly lit, in both Pavlovian (e.g. [42]) and operant paradigms (e.g. [22], [23], [24], [25]). However, lights have also been used as effective reinforcers during operant conditioning [2], [27], [14]. Experiment 1 aimed to determine whether a brief bright light serves as a punisher. If it does, making the light contingent on pressing one of two levers for food should reduce preference for that lever.
Experiment 2: escape/avoidance
Experiment 2 examined escape responses of albino rats using the operant burrow apparatus. The rates of head entries into the burrow were examined when a bright light was presented at various rates and durations, with entry terminating the light, and also when burrowing did not terminate the light. Given that each successful escape response produced an extended ITI, the present experiment also has a Sidman avoidance component.
Experiment 3: escape and avoidance
The escape paradigm used in Experiment 2 was replicated, with additional measures taken to eliminate temperature as a factor. The ability of bright light to support an avoidance response was then tested using the burrow apparatus.
General discussion
Our results demonstrate that light may bring behavior under aversive control within three paradigms: punishment, escape, and signaled avoidance. When rats had a choice between food and food plus light (Experiment 1), they displayed an unambiguous preference for food alone. When light was presented non-contingently (Experiments 2 and 3), rats escaped to an artificial burrow; this response was rarely emitted in the dark. Changes in the frequency (Experiment 1) and duration (Experiments 2 and 3)
Acknowledgments
This work was supported by NIDA-R01 DA006886 to Mark West (David J. Barker), Arizona State University-College of Liberal Arts and Sciences (Federico Sanabria), and NIMH-R01MH066860 (Peter Killeen). We thank Natalie Cole, Liliana Oldenburg, and Lara Olson for data collection.
References (46)
- et al.
Locus coeruleus activation by foot shock or electrical stimulation inhibits amygdala neurons
Neuroscience
(2007) - et al.
Long-term behavioural alterations in female rats after a single intense foot shock followed by situational reminders
Psychoneuroendocrinology
(2005) - et al.
Fear extinction in rats: implications for human brain imaging and anxiety disorders
Biol Psychol
(2006) - et al.
Double dissociating effects of sensory stimulation and cocaine on serotonin activity in the occipital and temporal cortices
Neuropharmacology
(2007) - et al.
Burrowing and feeding behaviour in the rat
Animal Behav
(1982) - et al.
Mesolimbic dopaminergic pathways in fear conditioning
Prog Neurobiol
(2004) - et al.
Light induced activity in the activity-box is not aversively motivated and does not show between-trial habituation
Physiol Behav
(2009) - et al.
Visual sensory-motor gating by serotonin activation in the medial prefrontal and occipital, but not in the rhinal, cortices in rats
Neuroscience
(2008) - et al.
Effect of contingent auditory stimuli on concurrent schedule performance: An alternative punisher to electric shock
Behav Processes
(2008) - et al.
Variations in illumination, closed wall transparency and/or extramaze space influence both baseline anxiety and response to diazepam in the rat elevated plus-maze
Behav Brain Res
(2009)
Effects of conditioned fear stress on 5-HT release in the rat prefrontal cortex
Pharmacol Biochem Behav
Concurrent observations of barpress suppression and freezing: effects of CS modality and on-line vs. off-line training upon posttrial behavior
Animal Learning Behav
Reinforcing effects of illumination change in different phases of the rat's diurnal cycle
J Comp Physiol Psychol
Antipredator defensive behaviors in a visible burrow system
J Comp Psychol
Species-specific defense reactions and avoidance learning
Psychol Rev
Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats
Behav Neurosci
Aversion thresholds and aversion difference limens for white light in albino and hooded rats
J Exp Psychol
Analysis of longitudinal data
A novel operant conflict procedure using incrementing shock intensities to assess the anxiolytics and anxiogenic effects of drugs
Behav Pharmacol
A progression for generating variable interval schedules
J Exp Anal Behav
Relation of cue to consequence in avoidance learning
Psychonomic Sci
Light stimulus change evokes an activity response in the rat
Learning Behav
Modulation of an activity response with associative and nonassociative fear in the rat: a lighting differential influences the form of defensive behavior evoked after fear conditioning
Learning Behav
Cited by (31)
Behavioural responses of anxiety in aversive and non-aversive conditions between young and aged Sprague-Dawley rats
2020, Behavioural Brain ResearchHarm to Others Acts as a Negative Reinforcer in Rats
2020, Current BiologyCitation Excerpt :In this view, harm aversion may not primarily be an altruistic motive to prevent pain to another rat but a more selfish motive to avoid an unpleasant personal state triggered by the signals emitted by the other rat—a less noble but perhaps equally effective motive. Indeed, rats can be motivated to switch their lever preference also against a panoply of non-social stimuli, including loud noises or bright light [50, 51]. By contrasting social and non-social stimuli, as has been done for vicarious freezing [20], an interesting question for future neuroscience research will be to investigate what brain structures may be specifically involved in modulating behavior based on the pain of others.
Aversive control of Betta splendens behavior using water disturbances: Effects of signaled and unsignaled free-operant avoidance and escape contingencies
2019, Behavioural ProcessesCitation Excerpt :The vast majority of research on learning and behavioral processes regulated by aversive contingencies employs electric-shock procedures typically with mammalian and avian animal models (e.g., fear conditioning, avoidance, and conditioned suppression – Cabrera and Dos Santos, 2012; Curzon et al., 2009; Hurtado-Parrado et al., 2017; Izquierdo et al., 2016; Kenney et al., 2017). This prevalence of electric shock in aversive control research with birds and mammals could be explained by its convenience of use, its reliability, its broad range of intensities and durations, the feasibility of titrating shock levels for individual subjects, and the fact that it is aversive at levels that do not cause tissue damage (Barker et al., 2010; Baron, 1991; Crosbie, 1998). In addition, electric shock can be presented very briefly so that processes such as avoidance and punishment can be studied independently of real or adventitiously reinforced escape behavior (Baron,1991; Sidman, 1953).
Repeated social defeat stress enhances the anxiogenic effect of bright light on operant reward-seeking behavior in rats
2015, Behavioural Brain Research
- 1
Tel.: +1 732 445 5405.