Donald A. Wilson

Habituation revisited: an updated and revised description of the behavioral characteristics of habituation.

The most commonly cited descriptions of the behavioral characteristics of habituation come from two papers published almost 40 years ago [Groves, P. M., & Thompson, R. F. (1970). Habituation: A dual-process theory. Psychological Review, 77, 419-450; Thompson, R. F., & Spencer, W. A. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychological Review, 73, 16-43]. In August 2007, the authors of this review, who study habituation in a wide range of species and paradigms, met to discuss their work on habituation and to revisit and refine the characteristics of habituation. This review offers a re-evaluation of the characteristics of habituation in light of these discussions. We made substantial changes to only a few of the characteristics, usually to add new information and expand upon the description rather than to substantially alter the original point. One additional characteristic, relating to long-term habituation, was added. This article thus provides a modern summary of the characteristics defining habituation, and can serve as a convenient primer for those whose research involves stimulus repetition.

Good memories of bad events in infancy.

If a helpless newborn infant does not form an attachment to its care-giver, even an abusive one, its chances of survival diminish, so evolution should strongly favour attachment by the infant, regardless of the quality of care-giving. As a part of the brain called the amygdala is critical for learned fear in adult animals, we investigated whether the development of learned avoidance behaviour could be delayed by late maturation of amygdala function. We found that very young rat pups exposed to various odours associated with shock treatment learn an approach response to that odour, whereas older pups learn odour avoidance. We show that the origin and development of learned odour-avoidance behaviour is associated with enhanced neural responses in the amygdala during odour-shock conditioning.

Neurobiology of associative learning in the neonate : early olfactory learning

Mammalian neonates have been simultaneously described as having particularly poor memory, as evidenced by infantile amnesia, and as being particularly excellent learners with unusually plastic nervous systems that are easily influenced by experience. An understanding of the neurobiological constraints and mechanisms of early learning may contribute to a unified explanation of these two disparate views. Toward that end, we review here our work on the neurobiology of learning and memory in neonates. Specifically, we have examined the neurobiology of early learning using an olfactory classical conditioning paradigm. Olfactory classical conditioning in neonates at the behavioral level conforms well with the requirements and outcomes of classical conditioning described in adults. Furthermore, specific neural correlates of this behavioral conditioning have been described including anatomical and physiological changes, neural pathways, and modulatory systems. In this Review, we outline the behavioral paradigm, the identified neural correlates, and apparent mechanisms of this learning. Finally, we compare the neurobiology of early learning with that reported for mature animals, with specific reference to the role of US-CS convergence, memory modulation, consolidation, and distributed memory.

Association of an Odor with Activation of Olfactory Bulb Noradrenergic β-Receptors or Locus Coeruleus Stimulation is Sufficient to Produce Learned Approach Responses to that Odor in Neonatal Rats

These experiments examined the sufficiency of pairing an odor with either intrabulbar activation of noradrenergic beta-receptors or pharmacological stimulation of the locus coeruleus to support learned odor preferences in Postnatal Day 6-7 rat pups. The results showed that pups exposed to odor paired with beta-receptor activation limited to the olfactory bulb (isoproterenol, 50 microM) displayed a conditioned approach response on subsequent exposure to that odor. Furthermore, putative stimulation of the locus coeruleus (2 microM idazoxan or 2 mM acetylcholine) paired with odor produced a subsequent preference for that odor. The effects of locus coeruleus stimulation could be blocked by a pretraining injection of the beta-receptor antagonist propranolol (20 mg/kg). Together these results suggest that convergence of odor input with norepinephrine release from the locus coeruleus terminals within the olfactory bulb is sufficient to support olfactory learning.

Olfactory perceptual learning: the critical role of memory in odor discrimination

The major problem in olfactory neuroscience is to determine how the brain discriminates one odorant from another. The traditional approach involves identifying how particular features of a chemical stimulus are represented in the olfactory system. However, this perspective is at odds with a growing body of evidence, from both neurobiology and psychology, which places primary emphasis on synthetic processing and experiential factors--perceptual learning--rather than on the structural features of the stimulus as critical for odor discrimination. In the present review of both psychological and sensory physiological data, we argue that the initial odorant feature extraction/analytical processing is not behaviorally/consciously accessible, but rather is a first necessary stage for subsequent cortical synthetic processing which in turn drives olfactory behavior. Cortical synthetic coding reflects an experience-dependent process that allows synthesis of novel co-occurring features, similar to processes used for visual object coding. Thus, we propose that experience and cortical plasticity are not only important for traditional associative olfactory memory (e.g. fear conditioning, maze learning, and delayed-match-to-sample paradigms), but also play a critical, defining role in odor discrimination.

Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex

Despite a remarkably precise spatial representation of odorant stimuli in the early stages of olfactory processing, the projections to the olfactory (piriform) cortex are more diffuse and show characteristics of a combinatorial array, with extensive overlap of afferent inputs and widespread intracortical association connections. Furthermore, although there is increasing evidence for the importance of temporal structure in olfactory bulb odorant-evoked output, little is known about how this temporal patterning is translated within cortical neural ensembles. The present study used multichannel electrode arrays and paired single-unit recordings in rat anterior piriform cortex to test several predictions regarding ensemble coding in this system. The results indicate that odorants evoke activity in a spatially scattered ensemble of anterior piriform cortex neurons, and the ensemble activity includes a rich temporal structure. The most pronounced discrimination between different odorants by cortical ensembles occurs during the first inhalation of a 2 s stimulus. The distributed spatial and temporal structure of cortical activity is present at both global and local scales, with neighboring single units contributing to coding of different odorants and active at different phases of the respiratory cycle. Finally, cross-correlogram analyses suggest that cortical unit activity reflects not only afferent input from the olfactory bulb but also intrinsic activity within the intracortical association fiber system. These results provide direct evidence for predictions stemming from anatomical- and theoretical-based models of piriform cortex.

The role of olfactory bulb norepinephrine in early olfactory learning.

Wistar rat pups were implanted with bilateral olfactory bulb cannulas on postnatal day 5 (PN5). On PN6, pups were trained in an olfactory classical conditioning task with peppermint odor as the CS and tactile stimulation/stroking as the UCS. Pups were randomly assigned to either PAIRED, BACKWARD or ODOR-only conditions. Half the pups in each group received intrabulbar infusions of 100 microM propranolol and half received intrabulbar infusions of saline during the training session. Propranolol infusions blocked acquisition of the learned odor preference expressed by PAIRED saline-infused pups. Diffusion of the infusate was checked in additional pups by infusing [3H]NE and performing LSC analysis. Infusate concentration did not significantly differ between the anterior and posterior halves of the bulb, but were sharply lower in the olfactory peduncle and more posterior areas. The results suggest that olfactory bulb NE is critical for early olfactory learning.

Separate encoding of identity and similarity of complex familiar odors in piriform cortex

Piriform cortical circuits are hypothesized to form perceptions from responses to specific odorant features, but the anterior piriform cortex (aPCX) and posterior piriform cortex (pPCX) differ markedly in their anatomical organization, differences that could lead to distinct roles in odor encoding. Here, we tested whether experience with a complex odorant mixture would modify encoding of the mixture and its components in aPCX and pPCX. Rats were exposed to an odorant mixture and its components in a go/no-go rewarded odor discrimination task. After reaching behavioral performance criterion, single-unit recordings were made from the aPCX and pPCX in these rats and in odor-naïve, control, urethane-anesthetized rats. After odor experience, aPCX neurons were more narrowly tuned to the test odorants, and there was a decorrelation in aPCX population responses to the mixture and its components, suggesting a more distinct encoding of the familiar mixture from its components. In contrast, pPCX neurons were more broadly tuned to the familiar odorants, and pPCX population responses to the mixture and its components became more highly correlated, suggesting a pPCX encoding of similarity between familiar stimuli. The results suggest aPCX and pPCX play different roles in the processing of familiar odors and are consistent with an experience-dependent encoding (perceptual learning) of synthetic odorant identity in aPCX and an experience-dependent encoding of odor similarity or odor quality in pPCX.

Plasticity in the Olfactory System: Lessons for the Neurobiology of Memory

We are rapidly advancing toward an understanding of the molecular events underlying odor transduction, mechanisms of spatiotemporal central odor processing, and neural correlates of olfactory perception and cognition. A thread running through each of these broad components that define olfaction appears to be their dynamic nature. How odors are processed, at both the behavioral and neural level, is heavily dependent on past experience, current environmental context, and internal state. The neural plasticity that allows this dynamic processing is expressed nearly ubiquitously in the olfactory pathway, from olfactory receptor neurons to the higher-order cortex, and includes mechanisms ranging from changes in membrane excitability to changes in synaptic efficacy to neurogenesis and apoptosis. This review will describe recent findings regarding plasticity in the mammalian olfactory system that are believed to have general relevance for understanding the neurobiology of memory.

Odour Perception: An Object-Recognition Approach

Object recognition is a crucial component of both visual and auditory perception. It is also critical for olfaction. Most odours are composed of 10s or 100s of volatile components, yet they are perceived as unitary perceptual events against a continually shifting olfactory background (ie figure—ground segregation). We argue here that this occurs by rapid central adaptation to background odours combined with a pattern-matching system to recognise discrete sets of spatial and temporal olfactory features—an odour object. We present supporting neuropsychological, learning, and developmental evidence and then describe the neural circuitry which underpins this. The vagaries of an object-recognition approach are then discussed, with emphasis on the putative importance of memory, multimodal representations, and top—down processing.