Whisking as a “voluntary” response: operant control of whisking parameters and effects of whisker denervation

The rat’s ability to vary its whisking “strategies” to meet the functional demands of a discriminative task suggests that whisking may be characterized as a “voluntary” behavior—an operant—and like other operants, should be modifiable by appropriate manipulations of response–reinforcer contingencies. To test this hypothesis we have used high-resolution, optoelectronic “real-time” recording procedures to monitor the movements of individual whiskers and reinforce specific movement parameters (amplitude, frequency). In one operant paradigm (N = 9) whisks with protractions above a specified amplitude were reinforced (Variable Interval 30?s) in the presence of a tone, but extinguished (EXT) in its absence. In a second paradigm (N = 3), rats were reinforced on two different VI schedules (VI-20s/VI-120s) signaled, respectively, by the presence or absence of the tone. Selective reinforcement of whisking movements maintained the behavior over many weeks of testing and brought it under stimulus and schedule control. Subjects in the first paradigm learned to increase responding in the presence of the tone and inhibit responding in its absence. In the second paradigm, subjects whisked at significantly different rates in the two stimulus conditions. Bilateral deafferentation of the whisker pad did not impair conditioned whisking or disrupt discrimination behavior. Our results confirm the hypothesis that rodent whisking has many of the properties of an operant response. The ability to bring whisking movement parameters under operant control should facilitate electrophysiological and lesion/behavioral studies of this widely used “model” sensorimotor system.     

Conditioned Whisking in the Rat

The rat's mystacial vibrissae are active during exploratory and discriminative behaviors, with individual vibrissae serving as elements in a receptive array scanned across object surfaces. To facilitate neurobehavioral analysis of this sensorimotor system, we have developed an experimental paradigm that confines vibrissa movements to a defined physical location, makes possible on-line monitoring of “whisking” activity, and brings such activity under associative control using operant conditioning procedures. Rats were secured, and movements of an identified bilaterally homologous pair of vibrissae (right and left gamma straddlers) were detected by laser-based photodetectors. Subjects were maintained on a water deprivation schedule, and whisker movements were monitored during adaptation to the test situation and after the clipping of other vibrissae on both sides of the snout. Rats were reinforced with water delivery for emitting vibrissa movements in the presence of a conditioned stimulus (tone) whose presentation was made contingent upon a prior period of nonwhisking. The rate and temporal distribution of vibrissa movements were brought under experimental control by means of interval and ratio reinforcement schedules. Although the procedures provide minimal information about the kinematics or topography of conditioned vibrissa movements, they permit the investigator to manipulate response parameters normally under the voluntary control of the animal in a preparation amenable to neurophysiological analysis     

Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks

We compared whisking movement patterns during acquisition of tactile detection and object discrimination under conditions in which (a) head movements are excluded and (b) exposure to tactile discriminanda is confined to the large, moveable vibrissae (macrovibrissae). We used optoelectronic instrumentation to track the movements of an individual whisker with high spatio-temporal resolution and a testing paradigm, which allowed us to dissociate performance on an "indicator" response (lever pressing) from the rat's "observing" responses (discriminative whisking). We analyzed the relation between discrimination performance and whisking movement patterns in order to clarify the process by which the indicator response comes under the stimulus control of information acquired by the rat's whisking behavior. Whisking patterns over the course of task acquisition differed with task demands. Acquisition of the Detection task was correlated with modulation of only one whisking movement parameter-total number of whisks emitted, and more whisking was seen on trials in which the discriminandum was absent. Discrimination between a sphere and cube differing in size and texture was correlated with a reduction in whisk duration and protraction amplitude and with a shift towards higher whisking frequencies. Our findings confirm previous reports that acquisition of tactile discriminations involves modulation by the animal of both the amount and the type of whisking. In contrast with a previous report (Brecht et al., 1997), they indicate that rats can solve tactile object detection and discrimination tasks (a) using only the large, motile mystacial vibrissae (macrovibrissae) and (b) without engaging in head movements. We conclude that the functional contribution of the macrovibrissae will vary with the nature of the task and the conditions of testing.     

Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks

We compared whisking movement patterns during acquisition of tactile detection and object discrimination under conditions in which (a) head movements are excluded and (b) exposure to tactile discriminanda is confined to the large, moveable vibrissae (macrovibrissae). We used optoelectronic instrumentation to track the movements of an individual whisker with high spatio-temporal resolution and a testing paradigm, which allowed us to dissociate performance on an “indicator” response (lever pressing) from the rat's “observing” responses (discriminative whisking). We analyzed the relation between discrimination performance and whisking movement patterns in order to clarify the process by which the indicator response comes under the stimulus control of information acquired by the rat's whisking behavior. Whisking patterns over the course of task acquisition differed with task demands. Acquisition of the Detection task was correlated with modulation of only one whisking movement parameter - total number of whisks emitted, and more whisking was seen on trials in which the discriminandum was absent. Discrimination between a sphere and cube differing in size and texture was correlated with a reduction in whisk duration and protraction amplitude and with a shift towards higher whisking frequencies. Our findings confirm previous reports that acquisition of tactile discriminations involves modulation by the animal of both the amount and the type of whisking. In contrast with a previous report (Brecht et al., 1997), they indicate that rats can solve tactile object detection and discrimination tasks (a) using only the large, motile mystacial vibrissae (macrovibrissae) and (b) without engaging in head movements.We conclude that the functional contribution of the macrovibrissae will vary with the nature of the task and the conditions of testing.     

Cortical barrel field ablation and unconditioned whisking kinematics

The effects of "barrel cortex" ablation upon the biometrics of "exploratory" whisking were examined in three head-fixed rats which had previously sustained unilateral ablation of the left cortical "barrel field" under electrophysiological control. Unconditioned movements of a pair of bilaterally homologous whiskers (C-1, Right, Left) were monitored, optoelectronically, with other whiskers present. Whisking movements on the intact and ablated side were analyzed with respect to kinematics (protraction amplitude and velocity) whisking frequency and phase relationships between whisking movement on the two sides of the face. Histological analysis confirmed complete removal of S-1 "barrel cortex". In normal animals whisking movements have a characteristic rhythm (6-9 Hz), and protractions on the two sides of the face tend to be both synchronous and of very similar amplitudes. In the lesioned animals, whisking frequency was unchanged and whisking movements remained bilaterally synchronous. However, there was a significant difference between the amplitude of Right and Left whisker movements which was evident many months postoperatively. Our results suggest that the deficits in vibrissa-mediated tactile discrimination reported after "barrel" field ablation may reflect an impairment in the animal's ability to modulate whisking parameters on the two sides of the face to meet the functional requirements of a discriminative whisking task. The effects upon whisking amplitude seen after unilateral barrel field ablation are consistent with a model in which the activity of a whisking Central Pattern Generator is modulated by descending inputs to achieve sensorimotor control of whisking movement parameters.     

Cortical barrel field ablation and unconditioned whisking kinematics

The effects of “barrel cortex” ablation upon the biometrics of “exploratory” whisking were examined in three head-fixed rats which had previously sustained unilateral ablation of the left cortical “barrel field” under electrophysiological control. Unconditioned movements of a pair of bilaterally homologous whiskers (C-1, Right, Left) were monitored, optoelectronically, with other whiskers present. Whisking movements on the intact and ablated side were analyzed with respect to kinematics (protraction amplitude and velocity) whisking frequency and phase relationships between whisking movement on the two sides of the face. Histological analysis confirmed complete removal of S-1 “barrel cortex”. In normal animals whisking movements have a characteristic rhythm (6-9 Hz), and protractions on the two sides of the face tend to be both synchronous and of very similar amplitudes. In the lesioned animals, whisking frequency was unchanged and whisking movements remained bilaterally synchronous. However, there was a significant difference between the amplitude of Right and Left whisker movements which was evident many months postoperatively. Our results suggest that the deficits in vibrissa-mediated tactile discrimination reported after “barrel” field ablation may reflect an impairment in the animal's ability to modulate whisking parameters on the two sides of the face to meet the functional requirements of a discriminative whisking task. The effects upon whisking amplitude seen after unilateral barrel field ablation are consistent with a model in which the activity of a whisking Central Pattern Generator is modulated by descending inputs to achieve sensorimotor control of whisking movement parameters.     

"Real-time" monitoring of vibrissa contacts during rodent whisking

Rodent whisking behavior provides active touch as input into a widely studied model system of information processing and behavior. We previously developed a simple optoelectronic system to monitor whisker movements in "real time" in head held rats at rest or performing various tasks such as tactile discrimination. We now describe a simple piezioelectic film device for detecting initial whisker contacts during whisking also in real time. In some applications this is as effective as high-speed videos and can be configured to isolate the contacts from different whiskers. The construction of this simple device is detailed. In addition to providing information during recordings from awake animals, the device could be used, for example, as an operant "manipulandum" for contingent reinforcement of object detection with a whisker.     

Topography of whisking II: interaction of whisker and pad

The peripheral effector system mediating rodent whisking produces protraction/retraction movements of the whiskers and translation movements of the collagenous mystacial pad. To examine the interaction of these movements during whisking in air we used high-resolution, optoelectronic methods for two-dimensional monitoring of whisker and pad movements in head-fixed rats. Under these testing conditions (1) whisker movements on the same side of the face are synchronous and of similar amplitude; (2) pad movements exhibit the characteristic 'exploratory' rhythm (6-12 Hz) of whisking but their movements often have a low frequency (1-2 Hz) component; (3) Pad movements occur in both antero-posterior and dorso-ventral planes but there are considerable variations in the amplitude and topography of movement parameters in the two planes. We conclude that (a) both whisker and pad receive input from a common central rhythm generator; (b) differences in whisker and pad amplitude and topography probably reflect differences in the biomechanical properties of the structures receiving that input; (c) pad movements make a significant contribution to the kinematics of whisking behavior and (d) the two-dimensional nature of pad translation movements significantly increases the rat's flexible control of its mobile sensor.     

Appetitive differential conditioning of the rabbit's jaw movement response. Effects of cue similarity and US magnitude

Two experiments examined appetitive differential conditioning of the rabbit's jaw movement response (JMR) in a two-phase procedure. The first phase entailed reinforced training with one conditioned stimulus (CS+), and the second phase involved intermixed presentations of CS+ and an unreinforced stimulus (CS-). In Experiment 1, CS+ was a 600-Hz tone, and CS- was either a 660-, 1,000-, or 2,100-Hz tone. In Experiment 2, the magnitude of the water unconditioned stimulus (US) paired with CS+ was either 1, 3, or 9 ml. The experiments revealed that 1) the level of responding to CS- rose for several days and then declined over the remainder of training; 2) the physical similarity between CS+ and CS- directly affected the level of responding to CS- but had no discernable effect on the level of responding to CS+; and 3) US magnitude positively affected the level of responding to CS+ and, to a lesser extent, CS-. The results are discussed in terms of their implications for Spence's gradient interaction theory and Pavlov's external inhibition hypothesis.     

Topography of rodent whisking--I. Two-dimensional monitoring of whisker movements

During 'active touch' the rodent whiskers scan the environment in a series of repetitive movements ('whisks') generating afferent signals which transform the spatial properties of objects into spatio-temporal patterns of neural activity. Based upon analyses carried out in a single movement plane, it has been generally assumed that these trajectories are essentially uni-dimensional, although more complex movements have been described in some rodents. The present study was designed to examine this assumption and to more precisely characterize whisking topography by monitoring whisking trajectories along both the antero-posterior and dorso-ventral axes. Using optoelectronic monitoring techniques with high-spatio-temporal resolution, movement data were obtained from a population of vibrissae sampled at different locations on the mystacial pad in head-fixed rats isolated from the perturbing effects of contact. For a substantial proportion of the population of whisking movements sampled, the trajectories generated by a single whisker is most accurately described as occupying an expended two-dimensional space in which the A-P component predominates. However, the whisker system exhibits a considerable range of trajectory types, suggesting a high degree of movement flexibility. For each vibrissa position, it was possible to delineate a 'trajectory' domain -- that portion of the animal's whisking space which is scanned by the movements of that vibrissa during whisking. Since the 'domains' of adjacent whiskers in the same row tend to overlap, synchronized movements of a subset of whiskers could generate a set of overlapping somatosensory fields analogous to overlapping retinal receptive fields. The organization of such trajectory domains within the rats' whisking space could provide the spatial component of the spatio-temporal integration process required to extract information about environmental features from the inputs generated by its recursive whisking movements.     

P300, probability,and the three-tone paradigm

The effects of stimulus probability on P300 from a 3-tone paradigm were examined in two experiments. Experiment 1 manipulated the probability of the non-target tone as 0.10, 0.45, or 0.80, while the target tone probability was always 0.10. Experiment 2 manipulated the probability of 3 tones as 0.10, 0.30, or 0.60, with one of the infrequent tones assigned as the target in each condition. Subjects were required to press a button in response to the target stimulus in both experiments. The results indicated that the P300 to the target and the non-target were both affected by the probability of the eliciting stimulus, such that component amplitude was inversely related to probability; no reliable P300 latency effects were found. Target tones elicited larger P300 amplitude than the non-target tones at the same probability. The findings suggest that probability effects on P300 amplitude are independent of responding to a specific target stimulus and are discussed with reference to the clinical utility of the 3-tone paradigm.     

Topography of rodent whisking--I. Two-dimensional monitoring of whisker movements

During 'active touch' the rodent whiskers scan the environment in a series of repetitive movements ('whisks') generating afferent signals which transform the spatial properties of objects into spatio-temporal patterns of neural activity. Based upon analyses carried out in a single movement plane, it has been generally assumed that these trajectories are essentially uni-dimensional, although more complex movements have been described in some rodents. The present study was designed to examine this assumption and to more precisely characterize whisking topography by monitoring whisking trajectories along both the antero-posterior and dorso-ventral axes. Using optoelectronic monitoring techniques with high-spatio-temporal resolution, movement data were obtained from a population of vibrissae sampled at different locations on the mystacial pad in head-fixed rats isolated from the perturbing effects of contact. For a substantial proportion of the population of whisking movements sampled, the trajectories generated by a single whisker is most accurately described as occupying an expended two-dimensional space in which the A-P component predominates. However, the whisker system exhibits a considerable range of trajectory types, suggesting a high degree of movement flexibility. For each vibrissa position, it was possible to delineate a 'trajectory' domain-that portion of the animal's whisking space which is scanned by the movements of that vibrissa during whisking. Since the 'domains' of adjacent whiskers in the same row tend to overlap, synchronized movements of a subset of whiskers could generate a set of overlapping somatosensory fields analogous to overlapping retinal receptive fields. The organization of such trajectory domains within the rats' whisking space could provide the spatial component of the spatio-temporal integration process required to extract information about environmental features from the inputs generated by its recursive whisking movements.     

Stimulus change dis-habituates operant responding supported by water reinforcers

The present experiment examined whether habituation contributes to within-session decreases in operant responding for water reinforcers. The experiment asked if this responding can be dishabituated, a fundamental property of habituated behavior. During baseline, rats’ lever pressing was reinforced by water on a variable interval 15-s schedule. During experimental conditions, rats responded on the same schedule and a new stimulus was introduced for 5 min at 15, 30 or 45 min into the 60-min session. The new stimulus was extinction, continuous reinforcement or flashing lights in different conditions. Rate of responding primarily decreased within the session during baseline. Introducing a new stimulus sometimes suppressed (extinction, continuous reinforcement) and sometimes increased (flashing lights) responding while it was in effect. The new stimulus increased responding after it ended and before it was presented in the session. The results are incompatible with the idea that non-habituation satiety factors (e.g., cellular hydration and blood volume) contributed to within-session changes in responding. These satiety factors should increase with increases in consumption, decrease with decreases in consumption and remain constant with constant consumption of water. Nevertheless, all stimulus changes increased operant responding for water. These results support the idea that habituation contributes to within-session decreases in responding for water reinforcers.     

Reinstatement of a food-maintained operant produced by compounding discriminative stimuli

After a tone and a light were established as discriminative stimuli for food-reinforced responding in rats, presenting these stimuli simultaneously produced over three times as many responses as either the tone or light alone. Following this stimulus compounding test, responses during the tone and during the light were not reinforced (extinction) for 20 sessions, essentially eliminating responding. On stimulus compounding tests administered after the 10th and 20th extinction sessions, tone-plus-light continued to produce significantly more responding than the tone or light alone. The compound even produced responses when the individual stimuli no longer did. These results suggest that the simultaneous presentation of multiple extinguished discriminative stimuli may also contribute to the reinstatement of other positively-reinforced behaviors, such as drug taking.     

P300-like potentials in the normal monkey using classical conditioning and an auditory ‘oddball’ paradigm

Endogenous components of evoked potentials resembling P300 in humans were sequentially studied in 3 cynomolgus monkeys (Macaca fascicularis) using an auditory ‘oddball’ paradigm. The two different auditory stimuli were 500 Hz and 4000 Hz tones, designated as the ‘frequent’ and ‘rare’ stimuli, respectively. The probability of ‘rare’ tone presentation was initially 0.2. We further used probabilities of 0.1, 0.3 and 0.5. The ‘rare’ stimulus was reinforced by electrical stimulation, which followed the onset of the high tone by 700 msec. After 3–5 training sessions, a late positive wave was observed following the ‘rare’ tone. The latency of this P300-like signal was 314±16.2 msec, and teh amplitude 23.6±3.14 μV. The amplitude of this potential was modified by changes in stimulus presentation probability and by withholding reinforcement.     

Relapse processes after the extinction of instrumental learning: renewal, resurgence, and reacquisition

It is widely recognized that extinction (the procedure in which a Pavlovian conditioned stimulus or an instrumental action is repeatedly presented without its reinforcer) weakens behavior without erasing the original learning. Most of the experiments that support this claim have focused on several "relapse" effects that occur after Pavlovian extinction, which collectively suggest that the original learning is saved through extinction. However, although such effects do occur after instrumental extinction, they have not been explored there in as much detail. This article reviews recent research in our laboratory that has investigated three relapse effects that occur after the extinction of instrumental (operant) learning. In renewal, responding returns after extinction when the behavior is tested in a different context; in resurgence, responding recovers when a second response that has been reinforced during extinction of the first is itself put on extinction; and in rapid reacquisition, extinguished responding returns rapidly when the response is reinforced again. The results provide new insights into extinction and relapse, and are consistent with principles that have been developed to explain extinction and relapse as they occur after Pavlovian conditioning. Extinction of instrumental learning, like Pavlovian learning, involves new learning that is relatively dependent on the context for expression.     

One whisker whisking: unit recording during conditioned whisking in rats

Understanding of the functional neurobiology of the rodent whisker system would be advanced by neurobehavioral studies in awake, behaving animals that combine unit recording from structures at various levels of the system with quantitative characterization of the kinematics and temporal organization of whisking. Such studies require the solution of a number of methodological problems. These include: chronic recording procedures ensuring unit isolation, stability and maximum yield, monitoring and display of unit activity and whisker movements within the same (ms) timeframe and behavioral paradigms which bring whisking movement parameters under the control of the experimenter rather than the rat. Here we describe a head-fixed rodent preparation which makes possible chronic recording of unit activity in the awake, whisking rat, combined with real-time, high resolution monitoring of whisker and pad movements in two dimensions and under behavioral control. While the head-fixed "whisking" preparation has some inherent limitations, it may be used to address a number of important neurobehavioral problems. We suggest that it should contribute significantly to understanding the functional neurobiology of the whisker system.     

Interstimulus interval as a discriminative stimulus: Evidence of the generality of a novel asymmetry in temporal discrimination learning

Three appetitive conditioning experiments with rats examined temporal discrimination learning within Pavlovian conditioning trials. In all experiments, the duration of a feature white noise stimulus signaled whether or not a subsequent 10-s target tone would be reinforced. In Experiment 1, the feature durations were 4 and 1 min. For one group of rats (Group 4+/1−), 4 min of noise signaled that the tone would be reinforced and 1 min of noise signaled that the tone would not be reinforced. A second group (Group 1+/4−) was trained with the reverse contingency. The results showed a clear asymmetry in temporal discrimination learning: rats trained with 4+/1− (Long+/Short−) learned the discrimination readily (responding more in the tone on reinforced than on nonreinforced trials), whereas rats trained with 1+/4− (Short+/Long) did not. In Experiment 2, the feature durations were shortened to 60 and 15 s. Due to strong excitatory conditioning of the 15-s feature, the reverse asymmetry was observed, with the Short+/Long− discrimination learned more readily than the Long+/Short− discrimination. However, Experiment 3 demonstrated that the original Long+/Short− advantage could be recovered while using 60− and 15-s feature durations if the excitatory conditioning of the feature was reduced by including nonreinforced feature trials. The results support previous research involving the timing of intertrial intervals and are consistent with the temporal elements hypothesis which holds that the passage of time is encoded as a series of hypothetical stimulus elements.     

Serotonin regulates rhythmic whisking

Many rodents explore their environment by rhythmically palpating objects with their mystacial whiskers. These rhythmic whisker movements ("whisking"; 5-9 Hz) are thought to be regulated by an unknown brainstem central pattern generator (CPG). We tested the hypothesis that serotonin (5-HT) inputs to whisking facial motoneurons (wFMNs) are part of this CPG. In response to exogenous serotonin, wFMNs recorded in vitro fire rhythmically at whisking frequencies, and selective 5-HT2 or 5-HT3 receptor antagonists suppress this rhythmic firing. In vivo, stimulation of brainstem serotonergic raphe nuclei evokes whisker movements. Unilateral infusion of selective 5-HT2 or 5-HT3 receptor antagonists suppresses ipsilateral whisking and substantially alters the frequencies and symmetry of whisker movements. These findings suggest that serotonin is both necessary and sufficient to generate rhythmic whisker movements and that serotonergic premotoneurons are part of a whisking CPG.     

Electromyographic activity of mystacial pad musculature during whisking behavior in the rat

Cinematographic measurements of whisker movements generated by behaving rats were compared with electromyographic (EMG) activity recorded simultaneously from mystacial pad musculature. Muscle activity consisted of repetitive bursts, each of which initiated a "whisking" cycle consisting of a protraction followed by a retraction. Protraction amplitude and velocity were directly proportional to the amount of EMG activity during forward whisker movement. Overtime, the intensity of muscle discharge determined the set point about which the vibrissae moved; higher levels of muscle activity resulted in a greater degree of overall whisker protraction. These findings are consistent with the known anatomy of the facial musculature and underscore the importance of whisker protraction in the acquisition of tactile information by the vibrissae.