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olfactory coding
and decoding
by ensembles of
neurons
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Mark Stopfer, PhD, Head, Unit on Sensory
Coding and Neural Ensembles Iori Ito, PhD, Postdoctoral
Fellow Nobuaki Tanaka, PhD, Postdoctoral Fellow Stacey Brown, MS, Technician April Chiriboga, BS, Technician Rose Chik Ying Ong, MS, Graduate
Student Kiriana Cowansage, College
Student Jaclyn Feldman, High School Student |
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All animals need to know what
is going on in the world around them; thus, brain mechanisms have evolved to gather
and organize the sensory information required to build transient and
sometimes enduring internal representations of the animals’
surroundings. Using relatively simple animals and focusing primarily on
olfaction, we combine electrophysiological, anatomical, behavioral, and other
techniques to examine the ways intact neural circuits, driven by sensory
stimuli, process information. In the past year, our research program has
started to investigate several topics of interest; among them are the
mechanisms, including the transient oscillatory synchronization and slow
temporal firing patterns of ensembles of neurons, that underlie information
coding and decoding; the process whereby multimodal stimuli are integrated
into unified perceptions; and the processes that determine innate sensory
preferences. Our work reveals basic mechanisms by which sensory information
is transformed, stabilized, and compared as it makes its way through the
nervous system. Representation of the
quality, quantity, and temporal properties of a stimulus by spatiotemporal
neural ensemble activity Brown, Stopfer Principle neurons of the
olfactory system respond to odor stimulation with elaborate patterns of
action potentials, consisting of sequences of excitation, inhibition, and
quiescence. Such patterns, which often outlast the odor encounter, have been
shown to contain information about the identity and concentration of the
odorant. Thus, the olfactory system employs the temporal domain to represent
odor quality and quantity. The question then arises as to how this
spatiotemporal mechanism encodes odors encountered as rapid trains of nearly
overlapping brief pulses, as might occur in a natural odor plume. We
addressed this question by delivering odor pulses to the antennae of intact
locusts while recording from several brain locations. Specifically, in adult
locusts, we made intracellular recordings from projection neurons (analogous
to mitral cells) and local neurons with simultaneous electroantennogram (EAG)
records as we delivered 100ms odor pulses in trains of (1) three pulses with
interpulse intervals of 500, 750, 1,000, and 1,250ms and (2) 10 pulses with
an interpulse interval of 500ms. Each pulse pattern randomly delivered blocks
of 10 trials (15sec intertrial interval). We found that odor responses of
antennal lobe neurons changed reliably and significantly with the position of
the odor pulse within the train. The change was caused, at least in part, by
projection neuron- and odor-specific periods of inhibition. For trains of three
pulses, in 64 percent of projection neuron-odor combinations, we found that
the numbers of odor pulse–elicited spikes changed significantly with
pulse position. For 27 percent of projection neuron–odor combinations
(in which single pulses elicited spikes), the projection neuron spiked in
response to each of the three pulses; for 23 percent, never to the last
pulse; for 22 percent, never to the first pulse. In most cases, we observed
these effects with 750 ms (or longer) interpulse intervals, times greatly
exceeding the duration of pulse-elicited EAG deflections. A projection
neuron’s response to pulse position could change with odor or
concentration, suggesting the absence of a separate channel for temporal
information. Over trains of 10 pulses, response amplitudes of EAGs and local
neurons decreased; however, numbers of spikes in projection neuron responses
doubled, perhaps reflecting decreased inhibition from local neurons. Thus,
the projection neuron ensemble response appears to contain several types of
information: the temporal properties of the odor stimulus in addition to its
identity and concentration. We are examining the coding and decoding of this
information by recording from many projection neurons simultaneously and
using multiunit “tetrode” techniques and by recording from
downstream, potential “decoder” neurons. Stopfer M, Jayaraman V, Laurent G. Intensity versus
identity coding in an olfactory system. Neuron
2003;39:1-20. Fast learning in the
first olfactory interneuronal relay Brown; in collaboration
with Bazhenov Recordings
in the locust antennal lobe have revealed activity-dependent,
stimulus-specific changes in projection and local neuron response patterns
over the course of repeated odor presentations. During the first few trials,
response intensity of projection neurons decreases while spike time precision
increases and coherent oscillations, absent at first, quickly emerge. We
investigated the possible significance of, and mechanisms underlying, this
odor learning phenomenon by using a computational model of the antennal lobe,
including realistic projection neurons and local neurons with sparse
connectivity and inputs. To test quantitative predictions arising from the
computational model, we presented to intact locusts sequences of odorants
varying in molecular structure and concentration while making local field
potential recordings from their mushroom bodies (a projection site of the
first olfactory interneuronal relay). Our study suggests that fast olfactory
learning results from activity-dependent synaptic facilitation and may
improve the signal/noise ratio for repeatedly encountered odor stimuli. Mechanisms underlying
odor-specific slow temporal neural firing patterns Ito The
olfactory system encodes information about odor identity and concentration in
the spatiotemporal firing patterns of ensembles of principle neurons. Using
electrophysiological and new pharmacological tools, we are working to
understand and manipulate the neural mechanisms underlying the generation of
these patterns. We will be able to investigate the information content of
different aspects of the ensemble representation by specifically manipulating
them while assessing downstream neuronal and behavioral results. Innate preferences for
food odorants Chiriboga, Cowansage,
Feldman Newborn, naive animals often
display sensory preferences, perhaps reflecting an innate template for
important stimuli. As a first step in a mechanistic analysis of innate
preferences, we studied odor preferences and odor learning in hatchling locusts
and newly eclosed moths, which were raised in our laboratory under carefully
controlled conditions. We tested newly hatched locusts in an open field box,
permitting them to move freely toward either of two targets: filter paper
that had been rubbed with fresh wheat grass or green paper that carried no
grass odor. Both targets were enclosed within wire screening to prevent the
hatchlings from directly contacting them. We found the hatchlings were
significantly more attracted to the grass odor, even though they had never
before encountered it. We also tested the ability of newly eclosed moths to
learn associations between flower odorants and odorants that are innately
repellent to adult moths. The concentrations of all odorants were adjusted to
elicit approximately equivalent electroantennogram responses, indicating
equivalently intense olfactory sensory neuron activation. Using a proboscis
extension reflex conditioning paradigm in which odor puffs were temporally
paired with sugar water, we found that moths could learn to associate both
odor types with the reward. However, moths learned the food odor association
significantly faster. The work demonstrates that
locusts and moths are born with knowledge of the olfactory world. Because
both animals are relatively simple and suitable for behavioral and
electrophysiological study, we will be able to investigate mechanisms
underlying innate coding of sensory information. Information
reformatting through multiple interneuronal relays in the olfactory system Tanaka Genetic techniques in Drosophila allow for the reliable, in vivo labeling and conditional,
temporary knockout of specific neurons and neuron types. By combining these
techniques with direct electrophysiological and behavioral studies, we will
examine, in intact animals and with realistic stimuli, how and to what
purpose information is reformatted as it moves through the brain. COLLABORATOR Maxim Bazhenov,
PhD, The Salk Institute, For further information, contact stopferm@mail.nih.gov |
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