skip to main content


Title: Novelty detection in early olfactory processing of the honey bee, Apis mellifera
Animals are constantly bombarded with stimuli, which presents a fundamental problem of sorting among pervasive uninformative stimuli and novel, possibly meaningful stimuli. We evaluated novelty detection behaviorally in honey bees as they position their antennae differentially in an air stream carrying familiar or novel odors. We then characterized neuronal responses to familiar and novel odors in the first synaptic integration center in the brain–the antennal lobes. We found that the neurons that exhibited stronger initial responses to the odor that was to be familiarized are the same units that later distinguish familiar and novel odors, independently of chemical identities. These units, including both tentative projection neurons and local neurons, showed a decreased response to the familiar odor but an increased response to the novel odor. Our results suggest that the antennal lobe may represent familiarity or novelty to an odor stimulus in addition to its chemical identity code. Therefore, the mechanisms for novelty detection may be present in early sensory processing, either as a result of local synaptic interaction or via feedback from higher brain centers.  more » « less
Award ID(s):
2014217
NSF-PAR ID:
10320890
Author(s) / Creator(s):
; ; ; ; ; ;
Editor(s):
Skoulakis, Efthimios M.
Date Published:
Journal Name:
PLOS ONE
Volume:
17
Issue:
3
ISSN:
1932-6203
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Animals depend on fast and reliable detection of novel stimuli in their environment. Neurons in multiple sensory areas respond more strongly to novel in comparison to familiar stimuli. Yet, it remains unclear which circuit, cellular, and synaptic mechanisms underlie those responses. Here, we show that spike-timing-dependent plasticity of inhibitory-to-excitatory synapses generates novelty responses in a recurrent spiking network model. Inhibitory plasticity increases the inhibition onto excitatory neurons tuned to familiar stimuli, while inhibition for novel stimuli remains low, leading to a network novelty response. The generation of novelty responses does not depend on the periodicity but rather on the distribution of presented stimuli. By including tuning of inhibitory neurons, the network further captures stimulus-specific adaptation. Finally, we suggest that disinhibition can control the amplification of novelty responses. Therefore, inhibitory plasticity provides a flexible, biologically plausible mechanism to detect the novelty of bottom-up stimuli, enabling us to make experimentally testable predictions. 
    more » « less
  2. Abstract

    The ability to identify odors in the environment is crucial for survival and reproduction. However, whether olfactory processing in higher-order brain centers is influenced by an animal’s physiological condition is unknown. We usedin vivoneuron and local field potential (LFP) recordings from the ventral telencephalon of dominant and subordinate male cichlids to test the hypothesis that response properties of olfactory neurons differ with social status. Dominant males had a high percentage of neurons that responded to several odor types, suggesting broad tuning or differential sensitivity when males are reproductively active and defending a territory. A greater percentage of neurons in dominant males also responded to sex- and food-related odors, while a greater percentage of neurons in subordinate males responded to complex odors collected from behaving dominant males, possibly as a mechanism to mediate social suppression and allow subordinates to identify opportunities to rise in rank. Odor-evoked LFP spectral densities, indicative of synaptic inputs, were also 2–3-fold greater in dominant males, demonstrating status-dependent differences in processing possibly linking olfactory and other neural inputs to goal-directed behaviors. For the first time we reveal social and reproductive-state plasticity in olfactory processing neurons in the vertebrate forebrain that are associated with status-specific lifestyles.

     
    more » « less
  3. Abstract

    Olfactory projection neurons convey information from the insect antennal lobe (AL) to higher brain centers. Previous reports have demonstrated that pheromone‐responsive projection neurons with cell bodies in the moth medial cell cluster (mcPNs) predominantly have dendritic arborizations in the sexually dimorphic macroglomerular complex (MGC) and send an axon from the AL to the calyces of the mushroom body (CA) as well as the lateral horn (LH) of the protocerebrum via the medial AL tract. These neurons typically exhibit a narrow odor tuning range related to the restriction of their dendritic arbors within a single glomerulus (uniglomerular). In this study, we report on the diverse physiological and morphological properties of a group of pheromone‐responsive olfactory projection neurons with cell bodies in the AL lateral cell cluster (MGClcPNs) of two closely related moth species. All pheromone‐responsivelcPNs appeared to exhibit “basket‐like” dendritic arborizations in two MGC compartments and made connections with various protocerebral targets including ventrolateral and superior neuropils via projections primarily through the lateral AL tract and to a lesser extent the mediolateral antennal lobe tract. Physiological characterization of MGClcPNs also revealed a diversity of response profiles including those either enhanced by or reliant upon presentation of a pheromone blend. These responses manifested themselves as higher maximum firing rates and/or improved temporal resolution of pulsatile stimuli. MGClcPNs therefore participate in conveying diverse olfactory information relating to qualitative and temporal facets of the pheromone stimulus to a more expansive number of protocerebral targets than theirmcPN counterparts.

     
    more » « less
  4. The transition to motherhood in mammals is marked by changes in females’ perception of and responsiveness to sensory stimuli from infants. Our understanding of maternally induced sensory plasticity relies most heavily on studies in uniparental, promiscuous house mice and rats, which may not be representative of rodent species with different life histories. We exposed biparental, monogamous California mouse (Peromyscus californicus) mothers and ovariectomized virgin females to one of four acoustic and olfactory stimulus combinations (Control: clean cotton and white noise; Call: clean cotton and pup vocalizations; Odor: pup-scented cotton and white noise; Call + Odor: pup-scented cotton and pup vocalizations) and quantified females’ behavior and Fos expression in select brain regions. Behavior did not differ between mothers and ovariectomized virgins. Among mothers, however, those exposed to the Control condition took the longest to sniff the odor stimulus, and mothers exposed to the Odor condition were quicker to sniff the odor ball compared to those in the Call condition. Behavior did not differ among ovariectomized virgins exposed to the different conditions. Fos expression differed across conditions only in the anterior hypothalamic nucleus (AHN), which responds to aversive stimuli: among mothers, the Control condition elicited the highest AHN Fos and Call + Odor elicited the lowest. Among ovariectomized virgin fe- males, Call elicited the lowest Fos in the AHN. Thus, reproductive status in California mice alters females’ behavioral responses to stimuli from pups, especially odors, and results in the inhibition of defense circuitry in response to pup stimuli. 
    more » « less
  5. Abstract

    Predator odors such as urine and feces are known to elicit antipredator behaviors in prey including avoidance, fear, and curiosity. We measured how wild brown mouse lemurs (Microcebus rufus) responded to odors of mammalian, avian, and snake predators as well as nonpredator controls. The first experiment took place under controlled conditions in a laboratory where we recorded the occurrence of four behavioral categories (ignore, curiosity, alert, and fear) in response to a single odor. Subjects exhibited behavioral change significantly more often in response to the predator than to control stimuli, but did not distinguish between familiar and unfamiliar predators. Mammalian predator urine and feces were most likely to elicit behavioral change. The owl was the only predator to never elicit behavioral change, possibly because owls do not provide relevant odor cues. A second experiment employing live traps in the forest found that neither predator nor control odors affected the likelihood of capture. Due to their longevity, odors do not provide accurate information of spatial and temporal risk, and while mouse lemurs may have initially hesitated to enter a trap, in the absence of additional information about risk, they may have eventually ignored the stimuli. This study found that brown mouse lemurs are able to distinguish between predator and nonpredator odors, and that risk assessment may be affected by the experience, as well as predator and sensory stimulus quality.

     
    more » « less