Neural Mechanisms of Selective Auditory Attention in Rats (Dissertation)

How does attention modulate sensory representations? In order to probe the underlying neural mechanisms, we established a simple rodent model of modality-specific attention. Rats were trained to perform distinct auditory two-tone discrimination and olfactory odor discrimination in a two alternative choice (2AC) paradigm. 
To determine auditory cortex’s role in this frequency discrimination task, we used GABA-A receptor agonist muscimol to transiently and reversibly inactivate auditory cortexes bilaterally in rats performing simple interleaved auditory and olfactory discrimination. With olfactory discrimination performance serving as internal control for motivation and decision making capability, we found only auditory two-tone discrimination was selectively impaired in these rats. This shows the auditory cortex is involved in this two-tone discrimination task.
To investigate the neural correlate of modality-specific attention in the auditory cortex, we trained rats to perform interleaved auditory and olfactory blocks (of 50~70 trials each) in a single session. In auditory blocks, pure tones were either presented with or without a neutral odor (caproic acid, n=2 and 3 respectively), and subjects were rewarded for discriminating auditory stimuli. In olfactory blocks, both task odors and pure tones were presented simultaneously, and subjects were rewarded for discriminating olfactory stimuli. We recorded neural responses in primary auditory cortex (area A1) in freely moving rats while subjects performed this behavior. Single unit responses to tones were heterogeneous, and included transient, sustained, and suppressed. We found 205 of 802 units recorded responsive to the stimuli we used. Of these 205 units, 18.5% showed modality-specific attentional modulation of the anticipatory activity before tone onset. In addition, we also observed in smaller proportion of units (11.2%) modality-specific attentional modulation of the tone-evoked responses; in most cases, the responses to a particular auditory stimulus was enhanced in the auditory block (or, equivalently, suppressed in the olfactory block). Attention increased choice probability of the population in the auditory block. We have also observed significant behavior choice probability in small proportions of units. 
Our results suggest that shifting attention between audition to olfaction tasks can modulate the activity of single neurons in primary auditory cortex

Neural mechanisms of social learning in the female mouse

Social interactions are often powerful drivers of learning. In female mice, mating creates a long-lasting sensory memory for the pheromones of the stud male that alters neuroendocrine responses to his chemosignals for many weeks. The cellular and synaptic correlates of pheromonal learning, however, remain unclear. We examined local circuit changes in the accessory olfactory bulb (AOB) using targeted ex vivo recordings of mating-activated neurons tagged with a fluorescent reporter. Imprinting led to striking plasticity in the intrinsic membrane excitability of projection neurons (mitral cells, MCs) that dramatically curtailed their responsiveness, suggesting a novel cellular substrate for pheromonal learning. Plasticity was selectively expressed in the MC ensembles activated by the stud male, consistent with formation of memories for specific individuals. Finally, MC excitability gained atypical activity-dependence whose slow dynamics strongly attenuated firing on timescales of several minutes. This unusual form of AOB plasticity may act to filter sustained or repetitive sensory signals.R21 DC013894 - NIDCD NIH HH

Neural Correlates of Social Behavior in Mushroom Body Extrinsic Neurons of the Honeybee Apis mellifera

The social behavior of honeybees (Apis mellifera) has been extensively investigated, but little is known about its neuronal correlates. We developed a method that allowed us to record extracellularly from mushroom body extrinsic neurons (MB ENs) in a freely moving bee within a small but functioning mini colony of approximately 1,000 bees. This study aimed to correlate the neuronal activity of multimodal high-order MB ENs with social behavior in a close to natural setting. The behavior of all bees in the colony was video recorded. The behavior of the recorded animal was compared with other hive mates and no significant differences were found. Changes in the spike rate appeared before, during or after social interactions. The time window of the strongest effect on spike rate changes ranged from 1 s to 2 s before and after the interaction, depending on the individual animal and recorded neuron. The highest spike rates occurred when the experimental animal was situated close to a hive mate. The variance of the spike rates was analyzed as a proxy for high order multi-unit processing. Comparing randomly selected time windows with those in which the recorded animal performed social interactions showed a significantly increased spike rate variance during social interactions. The experimental set-up employed for this study offers a powerful opportunity to correlate neuronal activity with intrinsically motivated behavior of socially interacting animals. We conclude that the recorded MB ENs are potentially involved in initiating and controlling social interactions in honeybees

Neuroethology of olfactory-guided behavior and its potential application in the control of harmful insects

Harmful insects include pests of crops and storage goods, and vectors of human and animal diseases. Throughout their history, humans have been fighting them using diverse methods. The fairly recent development of synthetic chemical insecticides promised efficient crop and health protection at a relatively low cost. However, the negative effects of those insecticides on human health and the environment, as well as the development of insect resistance, have been fueling the search for alternative control tools. New and promising alternative methods to fight harmful insects include the manipulation of their behavior using synthetic versions of "semiochemicals", which are natural volatile and non-volatile substances involved in the intra-and/or inter-specific communication between organisms. Synthetic semiochemicals can be used as trap baits to monitor the presence of insects, so that insecticide spraying can be planned rationally (i.e., only when and where insects are actually present). Other methods that use semiochemicals include insect annihilation by mass trapping, attract-and-kill techniques, behavioral disruption, and the use of repellents. In the last decades many investigations focused on the neural bases of insect's responses to semiochemicals. Those studies help understand how the olfactory system detects and processes information about odors, which could lead to the design of efficient control tools, including odor baits, repellents or ways to confound insects. Here we review our current knowledge about the neural mechanisms controlling olfactory responses to semiochemicals in harmful insects. We also discuss how this neuroethology approach can be used to design or improve pest/vector management strategies.Fil: Reisenman, Carolina Esther. University of California at Berkeley; Estados UnidosFil: Lei, Hong. University of Arizona; Estados UnidosFil: Guerenstein, Pablo Gustavo. Provincia de Entre Ríos. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción. Universidad Autónoma de Entre Ríos. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción; Argentina. Universidad Nacional de Entre Ríos. Facultad de Ingeniería; Argentin

The Chemical Senses

Long-standing neglect of the chemical senses in the philosophy of perception is due, mostly, to their being regarded as ‘lower’ senses. Smell, taste, and chemically irritated touch are thought to produce mere bodily sensations. However, empirically informed theories of perception can show how these senses lead to perception of objective properties, and why they cannot be treated as special cases of perception modelled on vision. The senses of taste, touch, and smell also combine to create unified perceptions of flavour. The nature of these multimodal experiences and the character of our awareness of them puts pressure on the traditional idea that each episode of perception goes one or other of the five senses. Thus, the chemical senses, far from being peripheral to the concerns of the philosophy of perception, may hold important clues to the multisensory nature of perception in general

Wine tasting: a neurophysiological measure of taste and olfaction interaction in the experience

In the last years have been provided evidences of sensory–sensory connectivity and influences of one modality over primary sensory cortex of another, a phenomena called crossmodality. Typically, for the wine tasting, sommeliers in addition to the use of the gustation, by the introduction of the wine into the mouth, employ the stimulation of the olfactory system both through a direct olfactory stimulation (by the nose) and a retro-nasal pathway (inhaling air while swirling the wine around in the mouth). Aim of the present study was to investigate the reaction to the wine gustation with and without the direct olfactory contribution, through an electroencephalographic index of approach or withdrawal (AW) motivation, and an autonomic index (Emotional Index – EI), deriving from the matching of heart rate and galvanic skin response activity and considered an indicator of emotional involvement. Results showed a statistically significant increase of the EI values in correspondence of wine tasting with the olfactory component (p<0.01) in comparison to the tasting without the direct olfactory contribution, and a trend of greater approach attitude was reported for the same condition. Data suggest an interaction of the two sensory modalities influencing the emotional and the cognitive aspects of wine tasting experience in a non-expert sampl

Fast and robust learning by reinforcement signals: explorations in the insect brain

We propose a model for pattern recognition in the insect brain. Departing from a well-known body of knowledge about the insect brain, we investigate which of the potentially present features may be useful to learn input patterns rapidly and in a stable manner. The plasticity underlying pattern recognition is situated in the insect mushroom bodies and requires an error signal to associate the stimulus with a proper response. As a proof of concept, we used our model insect brain to classify the well-known MNIST database of handwritten digits, a popular benchmark for classifiers. We show that the structural organization of the insect brain appears to be suitable for both fast learning of new stimuli and reasonable performance in stationary conditions. Furthermore, it is extremely robust to damage to the brain structures involved in sensory processing. Finally, we suggest that spatiotemporal dynamics can improve the level of confidence in a classification decision. The proposed approach allows testing the effect of hypothesized mechanisms rather than speculating on their benefit for system performance or confidence in its responses

Synaptophysin and synaptoporin expression in the developing rat olfactory system

The expressions of two closely related synaptic vesicle antigens synaptophysin and synaptoporin were examined in the olfactory system of the adult rat and during pre- and postnatal development. In the adult, immunocytochemistry showed that the continuously regenerating olfactory receptor neurons (primary neurons) produce both synaptophysin and synaptoporin which were localized in the cell bodies of the receptor neurons in the olfactory epithelium, their dendrites, axonal processes in the olfactory nerve and their terminals in the olfactory bulb glomeruli. Furthermore, ultrastructural analysis revealed synaptophysin- and synaptoporin-immunore activities associated with synaptic vesicles in most olfactory receptor axonal terminals impinging on dendrites of the mitral and tufted neurons (secondary neurons in the olfactory bulb circuitry) in the olfactory glomeruli. In like manner, tufted neurons, granule and periglomerular neurons (interneurons in the olfactory bulb circuitry) express both synaptophysin and synaptoporin. In contrast, mitral neurons expressed only the synaptophysin antigen which was likewise associated with mitral axonal terminals in their target the olfactory cortex. The patterns of synaptophysin and synaptoporin expressions in mitral neurons (synaptophysin only) and tufted neurons (synaptophysin and synaptoporin) were similar in prenatal, postnatal and adult rats as revealed by immunocytochemistry and in situ hybridization. However, the biosynthesis of synaptophysin and synaptoporin by granule and periglomerular neurons, olfactory bulb interneurons, occurred mainly postnatally

Fruit scent and observer colour vision shape food-selection strategies in wild capuchin monkeys

The senses play critical roles in helping animals evaluate foods, including fruits that can change both in colour and scent during ripening to attract frugivores. Although numerous studies have assessed the impact of colour on fruit selection, comparatively little is known about fruit scent and how olfactory and visual data are integrated during foraging. We combine 25 months of behavioural data on 75 wild, white-faced capuchins (Cebus imitator) with measurements of fruit colours and scents from 18 dietary plant species. We show that frequency of fruit-directed olfactory behaviour is positively correlated with increases in the volume of fruit odours produced during ripening. Monkeys with red-green colour blindness sniffed fruits more often, indicating that increased reliance on olfaction is a behavioural strategy that mitigates decreased capacity to detect red-green colour contrast. These results demonstrate a complex interaction among fruit traits, sensory capacities and foraging strategies, which help explain variation in primate behaviour.https://www.nature.com/articles/s41467-019-10250-9Published versio

Cognitive facilitation following intentional odor exposure

This paper reviews evidence that, in addition to incidental olfactory pollutants, intentional odor delivery can impact cognitive operations both positively and negatively. Evidence for cognitive facilitation/interference is reviewed alongside four potential explanations for odor-induced effects. It is concluded that the pharmacological properties of odors can induce changes in cognition. However, these effects can be accentuated/attenuated by the shift in mood following odor exposure, expectancy of cognitive effects, and cues to behavior via the contextual association with the odor. It is proposed that greater consideration is required in the intentional utilization of odors within both industrial and private locations, since differential effects are observed for odors with positive hedonic qualities