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Donald A Wilson

Publications and source records attributed to Donald A Wilson.

At least 19 recordsLinked to original sources
PubMed2006

Synaptic adaptation and odor-background segmentation.

Habituation is a form of non-associative memory that plays an important role in filtering stable or redundant inputs. The present study examines the contribution of habituation and cortical adaptation to odor-background segmentation. Segmentation of target odorants from background odorants is a fundamental computational requirement for the olfactory system. Recent electrophysiological data have shown that odor specific adaptation in piriform cortex neurons, mediated at least partially by synaptic adaptation between the olfactory bulb outputs and piriform cortex pyramidal cells, may provide an ideal mechanism for odor-background segmentation. This rapid synaptic adaptation acts as a filter to enhance cortical responsiveness to changing stimuli, while reducing responsiveness to static, potentially background stimuli. Using previously developed computational models of the olfactory system, we here show how synaptic adaptation at the olfactory bulb input to the piriform cortex, as demonstrated electrophysiologically, creates odor specific adaptation. We show how this known feature of olfactory cortical processing can contribute to adaptation to a background odor and to odor-background segmentation. We then show in a behavioral experiment that the odor-background segmentation is perceptually important and functions at the same time-scale as the synaptic adaptation observed between the olfactory bulb and cortex.

Adaptation, Physiological↗
PubMed2006

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.

Animals↗
PubMed2006

Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala.

Rat pups must learn maternal odor to support attachment behaviors, including nursing and orientation toward the mother. Neonates have a sensitive period for rapid, robust odor learning characterized by increased ability to learn odor preferences and decreased ability to learn odor aversions. Specifically, odor-0.5 mA shock association paradoxically causes an odor preference and coincident failure of amygdala activation in pups until postnatal day 10 (P10). Because sensitive-period termination coincides with a declining "stress hyporesponsive period" when corticosterone release is attenuated, we explored the role of corticosterone in sensitive-period termination. Odor was paired with 0.5 mA shock in either sensitive-period (P8) or postsensitive-period (P12) pups while manipulating corticosterone. We then assessed preference/aversion learning and the olfactory neural circuitry underlying its acquisition. Although sensitive-period control paired odor-shock pups learned an odor preference without amygdala participation, systemic (3 mg/kg, i.p.; 24 h and 30 min before training) or intra-amygdala corticosterone (50 or 100 ng; during training) permitted precocious odor-aversion learning and evoked amygdala neural activity similar to that expressed by older pups. In postsensitive-period (P12) pups, control paired odor-shock pups showed an odor aversion and amygdala activation, whereas corticosterone-depleted (adrenalectomized) paired odor-shock pups showed odor-preference learning and activation of an odor learning circuit characteristic of the sensitive period. Intra-amygdala corticosterone receptor antagonist (0.3 ng; during training) infused into postsensitive-period (P12) paired odor-shock pups also showed odor-preference learning. These results suggest corticosterone is important in sensitive-period termination and developmental emergence of olfactory fear conditioning, acting via the amygdala as a switch between fear and attraction. Because maternal stimulation of pups modulates the pups' endogenous corticosterone, this suggests maternal care quality may alter sensitive-period duration.

Adrenalectomy↗
PubMed2006

Cortical contributions to olfaction: plasticity and perception.

In most sensory systems, the sensory cortex is the place where sensation approaches perception. As described in this review, olfaction is no different. The olfactory system includes both primary and higher order cortical regions. These cortical structures perform computations that take highly analytical afferent input and synthesize it into configural odor objects. Cortical plasticity plays an important role in this synthesis and may underlie olfactory perceptual learning. Olfactory cortex is also involved in odor memory and association of odors with multimodal input and contexts. Finally, the olfactory cortex serves as an important sensory gate, modulating information throughput based on recent experience and behavioral state.

Animals↗
PubMed2006

The International Society for Developmental Psychobiology annual meeting symposium: Impact of early life experiences on brain and behavioral development.

Decades of research in the area of developmental psychobiology have shown that early life experience alters behavioral and brain development, which canalizes development to suit different environments. Recent methodological advances have begun to identify the mechanisms by which early life experiences cause these diverse adult outcomes. Here we present four different research programs that demonstrate the intricacies of early environmental influences on behavioral and brain development in both pathological and normal development. First, an animal model of schizophrenia is presented that suggests prenatal immune stimulation influences the postpubertal emergence of psychosis-related behavior in mice. Second, we describe a research program on infant rats that demonstrates how early odor learning has unique characteristics due to the unique functioning of the infant limbic system. Third, we present work on the rodent Octodon degus, which shows that early paternal and/or maternal deprivation alters development of limbic system synaptic density that corresponds to heightened emotionality. Fourth, a juvenile model of stress is presented that suggests this developmental period is important in determining adulthood emotional well being. The approach of each research program is strikingly different, yet all succeed in delineating a specific aspect of early development and its effects on infant and adult outcome that expands our understanding of the developmental impact of infant experiences on emotional and limbic system development. Together, these research programs suggest that the developing organism's developmental trajectory is influenced by environmental factors beginning in the fetus and extending through adolescence, although the specific timing and nature of the environmental influence has unique impact on adult mental health.

Animals↗
PubMed2005

Olfactory cortical adaptation facilitates detection of odors against background.

Detection and discrimination of odors generally, if not always, occurs against an odorous background. On any given inhalation, olfactory receptor neurons will be activated by features of both the target odorant and features of background stimuli. To identify a target odorant against a background therefore, the olfactory system must be capable of grouping a subset of features into an odor object distinct from the background. Our previous work has suggested that rapid homosynaptic depression of afferents to the anterior piriform cortex (aPCX) contributes to both cortical odor adaptation to prolonged stimulation and habituation of simple odor-evoked behaviors. We hypothesize here that this process may also contribute to figure-ground separation of a target odorant from background stimulation. Single-unit recordings were made from both mitral/tufted cells and aPCX neurons in urethan-anesthetized rats and mice. Single-unit responses to odorant stimuli and their binary mixtures were determined. One of the odorants was randomly selected as the background and presented for 50 s. Forty seconds after the onset of the background stimulus, the second target odorant was presented, producing a binary mixture. The results suggest that mitral/tufted cells continue to respond to the background odorant and, when the target odorant is presented, had response magnitudes similar to that evoked by the binary mixture. In contrast, aPCX neurons filter out the background stimulus while maintaining responses to the target stimulus. Thus the aPCX acts as a filter driven most strongly by changing stimuli, providing a potential mechanism for olfactory figure-ground separation and selective reading of olfactory bulb output.

Adaptation, Physiological↗
PubMed2005

Relative medial and dorsal cortex volume in relation to sex differences in spatial ecology of a snake population.

In non-avian reptiles the medial and dorsal cortices are putative homologues of the hippocampal formation in mammals and birds. Studies on mammals and birds commonly report neuro-ecological correlations between hippocampal volume and aspects of spatial ecology. We examined the relationship between putative homologous cortical volumes and spatial use in a population of the squamate reptile, Agkistrodon piscivorus, that exhibits sex differences in spatial use. Do male A. piscivorus that inhabit larger home ranges than females also have larger putative hippocampal volumes? Male and female brains were sectioned and digitized to quantify regional cortical volumes. Although sex differences in dorsal cortex volume were not observed, males had a significantly larger medial cortex relative to telencephalon volume. Similar to studies on mammals and birds, relative hippocampal or medial cortex volume was positively correlated with patterns of spatial use. We demonstrate volumetric sex differences within a reptilian putative hippocampal homologue.

Agkistrodon↗
PubMed2005

Ontogeny of cortical synaptic depression underlying olfactory sensory gating in the rat.

Sensory gating is the ability to filter irrelevant or redundant sensory input and is a critical function of all sensory systems that allows efficient processing of important stimuli. The present results demonstrate that a form of activity-dependent synaptic depression recently found to be involved in both cortical and behavioral olfactory sensory gating, is functional by at least the first postnatal week in the rat piriform cortex, and shares a common metabotropic glutamate receptor mechanism.

Animals↗
PubMed2005

Cortical metabotropic glutamate receptors contribute to habituation of a simple odor-evoked behavior.

Defining the circuits that are involved in production and cessation of specific behaviors is an ultimate goal of neuroscience. Short-term behavioral habituation is the response decrement observed in many behaviors that occurs during repeated presentation of non-reinforced stimuli. Within a number of invertebrate models of short-term behavioral habituation, depression of a defined synapse has been implicated as the mechanism. However, the synaptic mechanisms of short-term behavioral habituation have not been identified within mammals. We have shown previously that a presynaptic metabotropic glutamate receptor (mGluR)-dependent depression of synapses formed by olfactory bulb afferents to the piriform (olfactory) cortex significantly contributes to adaptation of cortical odor responses. Here we show that blockade of mGluRs within the olfactory cortex of awake, behaving rats diminishes habituation of a simple odor-induced behavior, strongly implicating a central mechanism for sensory gating in olfaction.

Animals↗
PubMed2005

High-frequency oscillations are not necessary for simple olfactory discriminations in young rats.

Individual olfactory bulb mitral/tufted cells respond preferentially to groups of molecularly similar odorants. Bulbar interneurons such as periglomerular and granule cells are thought to influence mitral/tufted odorant receptive fields through mechanisms such as lateral inhibition. The mitralgranule cell circuit is also important in the generation of the odor-evoked fast oscillations seen in the olfactory bulb local field potentials and hypothesized to be an important indicator of odor quality coding. Infant rats, however, lack a majority of these inhibitory interneurons until the second week of life. It is unclear if these developmental differences affect olfactory bulb odor coding or behavioral odor discrimination. The following experiments are aimed at better understanding odor coding and behavioral odor discrimination in the developing olfactory system. Single-unit recordings from mitral/tufted cells and local field-potential recordings from both the olfactory bulb and anterior piriform cortex were performed in freely breathing urethane-anesthetized rats (postnatal day 7 to adult). Age-dependent behavioral odor discrimination to a homologous series of ethyl esters was also examined using a cross-habituation paradigm. Odorants were equated in all experiments for concentration (150 ppm) using a flow dilution olfactometer. In concordance with the reduced interneuron population, local field potentials in neonates lacked detectable odor-evoked gamma-frequency oscillations that were observed in mature animals. However, mitral/tufted cell odorant receptive fields and behavioral odor discrimination did not significantly change, despite known substantial changes in local circuitry and neuronal populations, over the age range examined. The results suggest that high-frequency local field-potential oscillations do not reflect processes critical for simple odor discrimination.

Action Potentials↗
PubMed2004

Coordinate synaptic mechanisms contributing to olfactory cortical adaptation.

Anterior piriform cortex (aPCX) neurons rapidly filter repetitive odor stimuli despite relatively maintained input from mitral cells. This cortical adaptation is correlated with short-term depression of afferent synapses, in vivo. The purpose of this study was to elucidate mechanisms underlying this nonassociative neural plasticity using in vivo and in vitro preparations and to determine its role in cortical odor adaptation. Lateral olfactory tract (LOT)-evoked responses were recorded in rat aPCX coronal slices. Extracellular and intracellular potentials were recorded before and after simulated odor stimulation of the LOT. Results were compared with in vivo intracellular recordings from aPCX layer II/III neurons and field recordings in urethane-anesthetized rats stimulated with odorants. The onset, time course, and extent of LOT synaptic depression during both in vitro electrical and in vivo odorant stimulation methods were similar. Similar to the odor specificity of cortical odor adaptation in vivo, there was no evidence of heterosynaptic depression between independent inputs in vitro. In vitro evidence suggests at least two mechanisms contribute to this activity-dependent synaptic depression: a rapidly recovering presynaptic depression during the initial 10-20 sec of the post-train recovery period and a longer lasting (approximately 120 sec) depression that can be blocked by the metabotropic glutamate receptor (mGluR) II/III antagonist (RS)-alpha-cyclopropyl-4-phosphonophenylglycine (CPPG) and by the beta-adrenergic receptor agonist isoproterenol. Importantly, in line with the in vitro findings, both adaptation of odor responses in the beta (15-35 Hz) spectral range and the associated synaptic depression can also be blocked by intracortical infusion of CPPG in vivo.

Adaptation, Physiological↗
PubMed2003

Trans-neuronal regulation of cortical apoptosis in the adult rat olfactory system.

Previous work has identified a population of neurons within the anterior piriform cortex that undergo rapid apoptosis following de-afferentation by olfactory bulbectomy in adult rats. The specific initiation signal for apoptosis in this paradigm is unknown, but may include an activity-dependent trans-neuronal cascade. The present report examined the effect of adult-onset unilateral naris occlusion, which reduces olfactory bulb afferent excitation of piriform cortex, on apoptosis (terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling [TUNEL]) in the rat anterior piriform cortex. Adult Long-Evans hooded rats received unilateral naris occlusion or a control manipulation and were sacrificed after 1, 5, 7, 10 or 20 days later. For comparison, a second group of rats received a unilateral bulbectomy and were sacrificed 24 h later. Counts of TUNEL-stained cell profiles were performed for layers I/II and layer III of the anterior piriform cortex ipsilateral and contralateral to the manipulation. The results confirmed that unilateral bulbectomy produced a dramatic increase in TUNEL labeling in layers I/II of the ipsilateral piriform cortex 24 h after bulbectomy. Unilateral naris closure also produced enhanced TUNEL labeling, although the magnitude of the effect was less than that produced by bulbectomy, and enhanced TUNEL labeling was apparent both ipsilateral and contralateral to the sealed naris compared to controls. Deprivation-induced TUNEL labeling was detectable by 24 h post-closure, peaked at 5 days and was no different from controls by 20 days post-closure. Neither bulbectomy nor naris closure affected TUNEL labeling in layer III. Together, these results suggest that there is a population of superficial cells in piriform cortex whose survival is tightly regulated by sensory input.

Animals↗
PubMed2003

Olfactory bulb mitral-tufted cell plasticity: odorant-specific tuning reflects previous odorant exposure.

Olfactory system second-order neurons, mitral-tufted cells, have odorant receptive fields (ORFs) (molecular receptive ranges in odorant space for carbon chain length in organic odorant molecules). This study quantified several dimensions of these excitatory odorant receptive fields to novel odorants in rats and then examined the effects of passive odorant exposure on the shape of the ORF-tuning curve. ORFs for carbon chain length of novel ethyl esters (pure odorants that the animals had not been exposed to previously) were determined before and after a 50 sec prolonged exposure to one of the odorants. In response to novel odorants, quantitative analysis of mitral-tufted cell excitatory ORFs revealed that the median ORF width spanned 3-4 carbons, generally with a single-most excitatory odorant. Exposure to either the most excitatory odorant (ON-PEAK) or an odorant that was two carbons longer (OFF-PEAK) for 50 sec produced whole ORF suppression immediately after the end of the prolonged exposure, with the ON-PEAK exposure producing the greatest suppression. These results are consistent with a feature-detecting function for mitral-tufted cells. Redetermination of the ORF 15 and 60 min after the exposure revealed that OFF-PEAK exposure produced a reduction in responsiveness to the best odorant and an increase in responsiveness to the exposed odorant. In contrast, exposure to the ON-PEAK odorant or no odorant did not affect ORFs. Given that mitral-tufted cells receive exclusive excitatory input from olfactory receptor neurons expressing identical receptor proteins, it is hypothesized that experience-induced mitral-tufted cell ORF changes reflect modulation of lateral and centrifugal olfactory bulb circuits.

Action Potentials↗
PubMed2003

Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons.

Current views of odorant discrimination by the mammalian olfactory system suggest that the piriform cortex serves as a site of odor object synthesis. Given the enormous number of odorant feature combinations possible in nature, however, it seems unlikely that cortical synthetic receptive fields (RFs) are innate but rather require experience for their formation. The present experiment addressed two issues. First, we made a direct comparison of mitral/tufted cell and anterior piriform cortex (aPCX) neuron abilities to discriminate odorant mixtures from their components to further test whether aPCX neurons can treat collections of features different from the features themselves (synthetic coding). Second, we attempted to determine the minimum duration of experience necessary for formation of cortical synthetic RFs. Single-unit recordings were made from mitral/tufted cells and aPCX layer II/III neurons in urethan-anesthetized rats. Cross-habituation between novel binary mixtures and their novel components was used to determine odor discrimination abilities. The results suggest that after >/=50 s of experience with a binary mixture, aPCX neurons can discriminate the mixture from its components, whereas mitral/tufted cells cannot. However, when limited to 10 s of experience with the mixture, aPCX neurons appear similar to mitral/tufted cells and do not discriminate mixtures from components. These results suggest experience-dependent synthetic processing in aPCX and suggest an important role for perceptual learning in normal odor discrimination.

Action Potentials↗
PubMed2003

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.

Animals↗
PubMed2003

The fundamental role of memory in olfactory perception.

Current emphasis on odorant physiochemical features as the basis for perception largely ignores the synthetic and experience-dependent nature of olfaction. Olfaction is synthetic, as mammals have only limited ability to identify elements within even simple odor mixtures. Furthermore, olfaction is experience-bound, as exposure alone can significantly affect the extent to which stimuli can be discriminated. We propose that early analytical processing of odors is inaccessible at the behavioral level and that all odors are initially encoded as 'objects' in the piriform cortex. Moreover, we suggest that odor perception is wholly dependent on the integrity of this memory system and that its loss severely impairs normal perception.

Animals↗