Can Traditions Emerge from the Interaction of Stimulus Enhancement and Reinforcement Learning? An Experimental Model

The study of social learning in captivity and behavioral traditions in the wild are two burgeoning areas of research, but few empirical studies have tested how learning mechanisms produce emergent patterns of tradition. Studies have examined how social learning mechanisms that are cognitively complex and possessed by few species, such as imitation, result in traditional patterns, yet traditional patterns are also exhibited by species that may not possess such mechanisms. We propose an explicit model of how stimulus enhancement and reinforcement learning could interact to produce traditions. We tested the model experimentally with tufted capuchin monkeys (Cebus apella), which exhibit traditions in the wild but have rarely demonstrated imitative abilities in captive experiments. Monkeys showed both stimulus enhancement learning and a habitual bias to perform whichever behavior first obtained them a reward. These results support our model that simple social learning mechanisms combined with reinforcement can result in traditional patterns of behavior.     

Evolution of Canine Information Processing under Conditions of Natural and Artificial Selection

The paper first argues that under conditions of domestication animals are necessarily selected (incidentally or otherwise) for (1) responsitivity to a broad band of stimuli and (2) behavioral plasticity. The consequent tractability of domestic animals is contrasted with the stimulus-boundness and response stereotypy of the fixed action patterns observed in wild animal behavior. It is suggested that this difference accounts for the differential trainability of wolves and dogs. The second section of the paper presents observational evidence that although the wolf is not very amenable to instrumental conditioning, it possesses a highly developed capacity for observational learning. It is then noted that since observational learning requires recognition of means-ends relationships this conclusion is inconsistent with the claim that wolf behavior is largely instinct-bound. Finally, these conclusions are reconciled by hypothesizing that the wolf possesses a “duplex” information-processing system, a primitive “instinctual” system that mediates basic survival responses and a more recently acquired “cognitive” system that evolved as the wolt became a group hunter. Neurobehavioral and developmental comparisons of wolf and dog suggest that these two systems have become integrated into a single scheme in the course of the dog's domestication.     

Neural correlates of knowledge: stable representation of stimulus associations across variations in behavioral performance

Behavioral responses to a sensory stimulus are often guided by associative memories. These associations remain intact even when other factors determine behavior. The substrates of associative memory should therefore be identifiable by neuronal responses that are independent of behavioral choices. We tested this hypothesis using a paired-associates task in which monkeys learned arbitrary associations between pairs of visual stimuli. We examined the activity of neurons in inferior temporal cortex as the animals prepared to choose a remembered stimulus from a visual display. The activity of some neurons (22%) depended on the monkey's behavioral choice; but for a novel class of neurons (54%), activity reflected the stimulus that the monkey was instructed to choose, regardless of the behavioral response. These neurons appear to represent memorized stimulus associations that are stable across variations in behavioral performance. In addition, many neurons (74%) were modulated by the spatial arrangement of the stimuli in the display.     

Behavioral determination of stimulus pair discrimination of auditory acoustic and electrical stimuli using a classical conditioning and heart-rate approach

Acute animal preparations have been used in research prospectively investigating electrode designs and stimulation techniques for integration into neural auditory prostheses, such as auditory brainstem implants and auditory midbrain implants. While acute experiments can give initial insight to the effectiveness of the implant, testing the chronically implanted and awake animals provides the advantage of examining the psychophysical properties of the sensations induced using implanted devices. Several techniques such as reward-based operant conditioning, conditioned avoidance, or classical fear conditioning have been used to provide behavioral confirmation of detection of a relevant stimulus attribute. Selection of a technique involves balancing aspects including time efficiency (often poor in reward-based approaches), the ability to test a plurality of stimulus attributes simultaneously (limited in conditioned avoidance), and measure reliability of repeated stimuli (a potential constraint when physiological measures are employed). Here, a classical fear conditioning behavioral method is presented which may be used to simultaneously test both detection of a stimulus, and discrimination between two stimuli. Heart-rate is used as a measure of fear response, which reduces or eliminates the requirement for time-consuming video coding for freeze behaviour or other such measures (although such measures could be included to provide convergent evidence). Animals were conditioned using these techniques in three 2-hour conditioning sessions, each providing 48 stimulus trials. Subsequent 48-trial testing sessions were then used to test for detection of each stimulus in presented pairs, and test discrimination between the member stimuli of each pair. This behavioral method is presented in the context of its utilisation in auditory prosthetic research. The implantation of electrocardiogram telemetry devices is shown. Subsequent implantation of brain electrodes into the Cochlear Nucleus, guided by the monitoring of neural responses to acoustic stimuli, and the fixation of the electrode into place for chronic use is likewise shown.     

Human preferences for symmetry: subjective experience, cognitive conflict and cortical brain activity

This study examines the links between human perceptions, cognitive biases and neural processing of symmetrical stimuli. While preferences for symmetry have largely been examined in the context of disorders such as obsessive-compulsive disorder and autism spectrum disorders, we examine various these phenomena in non-clinical subjects and suggest that such preferences are distributed throughout the typical population as part of our cognitive and neural architecture. In Experiment 1, 82 young adults reported on the frequency of their obsessive-compulsive spectrum behaviors. Subjects also performed an emotional Stroop or variant of an Implicit Association Task (the OC-CIT) developed to assess cognitive biases for symmetry. Data not only reveal that subjects evidence a cognitive conflict when asked to match images of positive affect with asymmetrical stimuli, and disgust with symmetry, but also that their slowed reaction times when asked to do so were predicted by reports of OC behavior, particularly checking behavior. In Experiment 2, 26 participants were administered an oddball Event-Related Potential task specifically designed to assess sensitivity to symmetry as well as the OC-CIT. These data revealed that reaction times on the OC-CIT were strongly predicted by frontal electrode sites indicating faster processing of an asymmetrical stimulus (unparallel lines) relative to a symmetrical stimulus (parallel lines). The results point to an overall cognitive bias linking disgust with asymmetry and suggest that such cognitive biases are reflected in neural responses to symmetrical/asymmetrical stimuli.     

COGNITIVE ASPECTS OF DIFFERENCE TESTING: MEMORY AND INTERSTIMULUS DELAY

There are many ways in which a laboratory difference test differs from 'real life' discrimination of foods. One of these is the interval of time between tasting the two stimuli to be discriminated. To investigate this, judges performed same-different discrimination tests using a citrus flavored beverage as a medium. The time interval between tasting the standard and comparison stimuli was varied. In this initial study, short intervals of zero, 30, 60 s were examined. For judges unfamiltar with the stimuli, performance deteriorated as the time interval increased. For judges familiar with the stimuli, the zero time interval elicited best performance but there was no decrease in performance when the interval was increased from 30 to 60 s. The results were explained by hypothesizing different types of memory trace for the standard stimulus being utilized for comparison with the comparison stimulus.     

Associative interference between cues and between outcomes presented together and presented apart: an integration

In recent years, 'stimulus competition' in the study of acquired behavior has referred exclusively to (a) associative competition between cues trained in compound (e.g. overshadowing and blocking). Rarely cited are older experiments cast in the verbal learning tradition, now complemented with data from humans and rats in Pavlovian preparations, that demonstrate (b) competition between cues separately trained with a common outcome (i.e. proactive and retroactive interference). Similarly neglected are numerous examples of (c) competition between outcomes separately trained with a common cue within the verbal learning literature (also proactive and retroactive interference) as well as within the Pavlovian literature (i.e. counterconditioning). Recent data demonstrate (d) competition between outcomes trained in compound, thereby completing the four cells of a 2x2 matrix (competing stimuli trained together vs. trained apart and the competing stimuli being cues or outcomes) which highlights the ubiquitous nature of associative stimulus interference/competition. Most contemporary theories of acquired behavior can account for the phenomena in one or at most two cells of this matrix. Whether a common mechanism underlies the phenomena in all four cells of the matrix is currently unclear, but until such time as data preclude a common mechanism, parsimony encourages efforts to develop a model that encompasses all four cells. Here we offer a tentative model that addresses all four cells, albeit with two processes.     

Disentangling the nature of the nicotine stimulus

Learning involving interoceptive stimuli likely plays an important role in many diseases and psychopathologies. Within this area, there has been extensive research investigating the interoceptive stimulus effects of abused drugs. In this pursuit, behavioral pharmacologists have taken advantage of what is known about learning processes and adapted the techniques to investigate the behavioral and receptor mechanisms of drug stimuli. Of particular interest is the nicotine stimulus and the use of the two-lever operant drug discrimination task and the Pavlovian drug discriminated goal-tracking task. There is strong concordance between the two methods when using "standard" testing protocols that minimize learning on test days. For example, ABT-418, nornicotine, and varenicline all fully evoked nicotine-appropriate responding. Notably, research from our laboratory with the discriminated goal-tracking task has used an alternative testing protocol. This protocol assesses stimulus substitution based on how well extinction learning using a non-nicotine ligand transfers back to the nicotine stimulus. These findings challenge conclusions based on more "standard" testing procedures (e.g., ABT-418 is not nicotine-like). As a starting point, we propose Thurstone scaling as a quantitative method for more precisely comparing transfer of extinction across doses, experiments, and investigators. We close with a discussion of future research directions and potential implications of the research for understanding interoceptive stimuli.     

Neuroethology has pregnant agendas

Two of the many agendas of neuroethology are illustrated with examples. The first issue is what cells or assemblies of cells and what patterns of activity are sufficient to accomplish recognition of ethologically important stimulus configurations and initiation of behavioral action. The theme is the opportunities available in relatively neglected approaches to these objectives. As an example, the approach is developed of gentle microstimulation of loci in the brain where cells have been found to be responsive to complex, natural stimuli, under conditions conducive to the performance of tell-tale behavior. Other approaches include: (a) microinjection of modulatory substances into regions with such complex recognition cells, and (b) recording in efficient and informative ways, by using multiple electrode arrays, registering wideband activity, in behaving animals. The second issue is what brain and behavior differences has evolution produced between major taxa at distinct grades of complexity. Emphasized are our relative ignorance of basic aspects of connectivity, physiology and cognitive capacities in the major grades and the probability of surprises from new studies that employ comparison. Accepted: 29 January 1999     

Vasotocin stimulates appetitive responses to the visual and pheromonal stimuli used by male roughskin newts during courtship

It is now well established that vasotocin (AVT) and its mammalian homologue vasopressin influence various social behaviors in vertebrates, but less is known about the mechanisms through which these peptides modulate behavior. In male roughskin newts, Taricha granulosa, AVT stimulates a courtship behavior, amplectic clasping. Three general explanations for how AVT affects male courtship behavior have been considered: by enhancing a central state of sexual motivation, by affecting sensorimotor integration mechanisms in individual sensory modalities, or by influencing a nonspecific state of attention, arousal, or anxiety. AVT administration enhanced appetitive responses to visual and olfactory sexual stimuli, as would be expected if AVT affects a state of sexual motivation that affects behavioral responses to sexual stimuli regardless of the sensory modality in which they are processed. However, AVT selectively enhanced responses to female olfactory stimuli (sex pheromones), but similarly enhanced responses to female and food-related visual stimuli (worms), thus questioning the utility of such a motivational mechanism, as responses to female stimuli were not selectively enhanced in all sensory modalities. We therefore propose that exogenous AVT independently influences olfactory processes associated with orientation/attraction toward a female sex pheromone and visual processes associated with orientation/attraction toward a visual feature common to females and worms. In further experiments AVT administration failed to stimulate feeding behavior but did decrease locomotor activity. Thus, AVT does not stimulate courtship behavior in this species by enhancing the animals' general state of attention or by decreasing general anxiety, as responses to nonsexual, attractive stimuli were not uniformly enhanced, nor by stimulating general arousal, as activity levels did not increase. Rather, the data support the conclusion that AVT affects courtship by influencing specific sensorimotor processes associated with behavioral responses to individual releasing stimuli, which suggests a mechanistic framework for understanding socially motivated behavior is this species.     

Good vibrations

How and where the brain forms associations between sensation and action are crucial questions in the field of cognitive neuroscience. In this issue of Neuron, add to an already impressive body of work elucidating the neural mechanisms responsible for forming categorical decisions about vibrotactile stimuli that guide behavior. Here they show that single neurons in premotor cortex represent, remarkably, what appears to be the entire temporal evolution of the decision process-from representation of the sensory stimulus, to formation of the discrimination, to the choice of behavioral output.     

A variable-response model for parasitoid foraging behavior

An important factor inducing variability in foraging behavior in parasitic wasps is experience gained by the insect. Together with the insect's genetic constitution and physiological state, experience ultimately defines the behavioral repertoire under specified environmental circumstances. We present a conceptual variable-response model based on several major observations of a foraging parasitoid's responses to stimuli involved in the hostfinding process. These major observations are that (1) different stimuli evoke different responses or levels of response, (2) strong responses are less variable than weak ones, (3) learning can change response levels, (4) learning increases originally low responses more than originally high responses, and (5) hostderived stimuli serve as rewards in associative learning of other stimuli. The model specifies how the intrinsic variability of a response will depend on the magnitude of the response and predicts when and how learning will modify the insect's behavior. Additional hypotheses related to the model concern how experience with a stimulus modifies behavioral responses to other stimuli, how animals respond in multistimulus situations, which stimuli act to reinforce behavioral responses to other stimuli in the learning process, and finally, how generalist and specialist species differ in their behavioral plasticity. We postulate that insight into behavioral variability in the foraging behavior of natural enemies may be a help, if not a prerequisite, for the efficient application of parasitoids in pest management.     

P3 responses to prosodic stimuli in adult autistic subjects

Autistic persons are known to have serious abnormalities in speech prosody. The present study attempted to ascertain whether autistic persons could discriminate and/or recognize prosodic contrasts in auditory stimuli. A group of 11 adult autistic subjects with normal IQ and an age-matched group of normal subjects were studied electrophysiologically and behaviorally during presentations of prosodic and phonemic stimuli. The cognitive P3 potential was recorded in response to rare (20%)/frequent (80%) presentations of phonemic stimuli, ‘ba/pa’, linguistic-prosodic stimuli, ‘Bob’. (statement)/‘Bob?’ (question), and emotional-prosodic stimuli, ‘Bob’ (happy)/‘Bob’ (happy)/’Bob’ (angry). Behaviorally, auditory discrimination was tested by requiring a button-press response to each presentation of the rare target stimulus and cognitive association was tested by requiring a match between the verbalized stimulus and an appropriate picture/word.Contrary to our hypothesis, the autistic subjects generally showed normal P3 responses to all stimuli and performed at a normal level in all behavioral tests. However, a significant autistic P3 response to the phoneme ‘pa’ was not demonstrated. This surprising result was reexamined and shown to reflect an unusually large autistic response to ‘pa’ as the frequent stimulus in the first recording block, this initial hyper-reactivity prevented a ‘frequent/rare’ differential when ‘pa’ was presented as the rare stimulus in a later recording block. In the P3 latency window, both the autistic and control groups showed the largest amplitude responses to emotional-prosodic stimuli; neither the N1 nor P2 showed these stimulus effects. Thus, ‘emotional sounds’ appear to be particularly effective in activating the neural substrate of the P3 generator system.Overall, these data indicate remarkably normal P3 and behavioral processing of prosodic stimuli by the high-functioning autistic subjects of this study.     

Ecological frames of mind: the role of cognition in behavioral ecology.

Cognitive psychology is the study of how information, from the senses and from memory, is used in the production of behavior. Investigation of the specifics of behavioral adaptation has already led some behavioral ecologists into the domain of animal cognition. I make several arguments for the benefits and the necessity of a sophisticated assessment by ecologists of the cognitive aspects of behavioral adaptation. First, because cognition typically serves to produce adaptive behavior, cognitive structure and function should reflect ecological demands; studies of cognition in ecological contexts are opportunities to understand adaptation. Furthermore, constraints on cognitive properties may help determine how behavior meets the environment. Studies of spatial memory in food-caching corvids exemplify how cognitive aspects of behavior may both reflect and determine specifics of adaptation. Second, many models in behavioral ecology assume certain cognitive abilities, such as timing or counting. Cognitive theory and methodology should be used to determine whether animals possess these abilities. I have provided examples. Third, consideration of cognitive function can lead to original ideas about the details of behavioral adaptation. Without a thorough integration of cognitive psychology with behavioral ecology, our understanding of the relation between behavior and selective pressures will be compromised.     

Quantitative analyses of observing and attending

We review recent experiments examining whether simple models of the allocation and persistence of operant behavior are applicable to attending. In one series of experiments, observing responses of pigeons were used as an analog of attending. Maintenance of observing is often attributed to the conditioned reinforcing effects of a food-correlated stimulus (i.e., S+), so these experiments also may inform our understanding of conditioned reinforcement. Rates and allocations of observing were governed by rates of food or S+ delivery in a manner consistent with the matching law. Resistance to change of observing was well described by behavioral momentum theory only when rates of primary reinforcement in the context were considered. Rate and value of S+ deliveries did not affect resistance to change. Thus, persistence of attending to stimuli appears to be governed by primary reinforcement rates in the training context rather than conditioned reinforcing effects of the stimuli. An additional implication of these findings is that conditioned "reinforcers" may affect response rates through some mechanism other than response-strengthening. In a second series of experiments, we examined the applicability of the matching law to the allocation of attending to the elements of compound stimuli in a divided-attention task. The generalized matching law described performance well, and sensitivity to relative reinforcement varied with sample duration. The bias and sensitivity terms of the generalized matching law may provide measures of stimulus-driven and goal-driven control of divided attention. Further application of theories of operant behavior to performance on attention tasks may provide insights into what is referred to variously as endogenous, top-down, or goal-directed control of attention.     

Asymmetries in stimulus comparisons by monkey and man

Similarity is a core concept in theories of object recognition, categorization, and reasoning. It is often conceptualized as a geometric distance in a multidimensional stimulus space. However, research in humans has revealed that similarity judgments involve more than a simple distance calculation and tend to be asymmetric when stimuli differ in factors such as prototypicality. For example, most people judge 99 to be more similar to 100 than 100 to 99. Up to now, it was not known whether such asymmetries might also occur in nonhuman subjects. This study reveals asymmetries in the pattern of errors made by four rhesus monkeys in a temporal same/different task. Monkeys usually perceived a smaller difference between two different stimuli when the first stimulus in a trial was less prototypical than the second, just as what was found previously for human subjects. The pattern of asymmetries differed between monkeys, and a control study showed that such variability is also present for human subjects. We propose that known neurophysiological mechanisms can account for asymmetry in the stimulus comparisons of both species. Thus, seemingly complex phenomena that occur when human subjects rate stimulus similarity are also present in macaques' similarity judgments and could be based on relatively simple mechanisms.     

Genetic Control of Startle Behavior in Medaka Fish

Genetic polymorphisms are thought to generate intraspecific behavioral diversities, both within and among populations. The mechanisms underlying genetic control of behavioral properties, however, remain unclear in wild-type vertebrates, including humans. To explore this issue, we used diverse inbred strains of medaka fish (Oryzias latipes) established from the same and different local populations. Medaka exhibit a startle response to a visual stimulus (extinction of illumination) by rapidly bending their bodies (C-start) 20-ms after the stimulus presentation. We measured the rates of the response to repeated stimuli (1-s interval, 40 times) among four inbred strains, HNI-I, HNI-II, HO5, and Hd-rR-II1, and quantified two properties of the startle response: sensitivity (response rate to the first stimulus) and attenuation of the response probability with repeated stimulus presentation. Among the four strains, the greatest differences in these properties were detected between HNI-II and Hd-rR-II1. HNI-II exhibited high sensitivity (approximately 80%) and no attenuation, while Hd-rR-II1 exhibited low sensitivity (approximately 50%) and almost complete attenuation after only five stimulus presentations. Our findings suggested behavioral diversity of the startle response within a local population as well as among different populations. Linkage analysis with F2 progeny between HNI-II and Hd-rR-II1 detected quantitative trait loci (QTL) highly related to attenuation, but not to sensitivity, with a maximum logarithm of odds score of 11.82 on linkage group 16. The three genotypes (homozygous for HNI-II and Hd-rR-II1 alleles, and heterozygous) at the marker nearest the QTL correlated with attenuation. Our findings are the first to suggest that a single genomic region might be sufficient to generate individual differences in startle behavior between wild-type strains. Further identification of genetic polymorphisms that define the behavioral trait will contribute to our understanding of the neural mechanisms underlying behavioral diversity, allowing us to investigate the adaptive significance of intraspecific behavioral polymorphisms of the startle response.     

Carving the cognitive niche: optimal learning strategies in homogeneous and heterogeneous environments

A model learning system is constructed, in which an organism samples behaviors from a behavioral repertoire in response to a stimulus and selects the behavior with the highest payoff. The stimulus and most rewarding behavior may be kept in the organism's long-term memory and reused if the stimulus is encountered again. The value of the memory depends on the reliability of the stimulus, that is, how the corresponding payoffs of behaviors change over time. We describe how the inclusion of memory can increase the optimal sampling size in environments with some stimulus reliability. In addition to using memory to guide behavior, our organism may use information in its memory to choose the stimulus to which it reacts. This choice is influenced by both the organism's memory state and how many stimuli the organism can observe (its sensory capability). The number of sampled behaviors, memory length, and sensory capability are the variables that define the learning strategy. When all stimuli have the same reliability, there appears to be only a single optimal learning strategy. However, when there is heterogeneity in stimulus reliability, multiple locally optimal strategies may exist.