Hans Liljenström (ed.)Advances in Cognitive Neurodynamics (IV)Advances in Cognitive Neurodynamics10.1007/978-94-017-9548-7_70

Active Behaviors in Odor Sampling Constrain the Task for Cortical Processing

Leslie M. Kay^{1, 2, 3}, Daniel Rojas-Líbano^{2, 3, 4} and Donald Frederick^{1, 3}

(1)

Department of Psychology, The University of Chicago, Chicago, IL, USA

(2)

Committee on Neurobiology, The University of Chicago, Chicago, IL, USA

(3)

Institute for Mind and Biology, The University of Chicago, Chicago, IL, USA

(4)

Instituto de Ciencias Biomédicas, Universidad de Chile, Santiago, Chile

Leslie M. Kay

Email: LKay@uchicago.edu

Abstract

Sensory perception is accomplished by means of active behaviors that help to extract information from the external environment. These behaviors become a part of the percept and also constrain the perceptual task. In olfactory perception, sniffing is the means by which individuals acquire olfactory stimuli from the environment. Rats sniff at 8–10 Hz during odor sampling, but each sniff has a different and stereotyped pattern that serves to find needed information. Higher flow sniffs are used to identify high sorption odors within mixtures, while lower flow sniffs are used to find lower sorption odors. Extended sniffing bouts (mean of 300–600 ms) are also stereotyped and tuned by the context in which rats identify odors. These sniffing bouts may be determined by the cognitive demands of the task or by particularities associated with training.

Keywords

Olfactory perceptionSniffingSorptivenessOdor samplingOdor discrimination

1 Introduction

Cortical sensory systems have been shown to employ various strategies to represent and process sensory information. In many systems precise temporal structure in neuronal firing patterns produce oscillations at the population level that occur in the process of discriminating or recognizing stimuli. Neural oscillations have been ascribed many functions by neuroscientists, from binding of diverse sensory features to attention to pattern separation. In the rat olfactory system, neurons in the olfactory bulb respond with a collective fast oscillation in the gamma frequency range (40–100 Hz) when an individual sniffs an odor in many contexts [1]. We assume that all the precision is accounted for by the neural activity in these systems, but we often fail to acknowledge that animals in any waking behavioral state engage in volitional and goal-directed behavior while actively seeking stimuli. These behaviors adjust the incoming sensory information according to the animal’s behavioral or cognitive goal, and they may be used to simplify or constrain the task for neurons in the brain. Behavioral effects on stimulus acquisition are well established in the visual arena, where investigators employ fixation strategies to normalize the sensory input. Here we summarize recent studies that address sniffing strategies in rodents; instead of normalizing out the sniff we describe emerging behavioral motifs for olfactory discrimination behavior. We address dynamics in behavior at the level of the single sniff and the sniffing bout. Single sniffs in the 7–10 Hz range have a period of 100–140 ms, while sniffing bouts composed of two to five sniffs generally range from 200 to 700 ms. Characterizing these highly dynamic behaviors is essential for understanding how odors are perceived.

2 Sorption and Sniffing Behavior

2.1 The Chromatographic Hypothesis

When odorant molecules pass over two media, such as air and mucus (as happens in the nose), they distribute between them. The sorptiveness of an odorant, quantified by the partition coefficient, describes this distribution. Besides this coefficient, the airflow at which the odorant passes over the mucus also determines how much odorant is absorbed. Faster flows cause fewer molecules to be absorbed compared to slower flows. In addition, areas of the sensory nasal epithelium that normally sustain lower airflows express a broad class of receptors that may bind low sorption odorants [2, 3]. Work by Mozell and colleagues showed that the olfactory epithelium functions as a kind of chromatograph, in which odorants strike preferentially at different zones of the epithelium depending on their sorptiveness [4, 5]. Given the abovementioned role of airflow in the odorant distribution, it has been suggested that animals may manipulate airflow through changes in sniffing to direct odorants to the epithelium zone where they are best detected [6].

2.2 Testing the Hypothesis (Methods)

We tested the chromatographic hypothesis in an experiment designed to challenge rats to identify an odorant within a binary mixture [7]. Because rats are extremely good at detecting odors, we wanted to test two rat groups, where both had to sniff the very same odor mixtures but each had to search within each mixture for specific odorants (that we called targets) of different sorptiveness for each group. We produced two sets of four monomolecular odorants, and in each set there were two high sorption and two low sorption odorants. Two groups of eight rats were trained to discriminate two novel training odors in a go/no-go task (sniff in a central odor port, then perform a nose poke in a second port for one odor, withhold responding for the other odor). After training, one rat group was assigned to find a high sorption target odor in the six binary mixtures formed from the odor set, and the other rat group was assigned to search for a low sorption odor in the same mixtures. They learned the target odor at the beginning of the session, and then they responded to randomly presented mixtures or the target odor. We repeated this for the second set of four odors, but the rat groups had their targets reversed (low sorption for the previously high sorption group, and vice versa). In addition to behavior, we also recorded EMG activity from the diaphragm muscle for each rat. This allowed us to estimate the relative airflow used for different sniffs, odors and days.

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