Biology subjects

Gire, D. H.

Publications and source records attributed to Gire, D. H..

11 recordsLinked to original sources

bioRxiv2024

Octopus can use odor plumes to find food

Odor-plume-guided navigation, tracking an odor plume to its source, is a primordial behavior used by most animals to search beyond the visual range. Here we report the first laboratory observations of octopuses performing this behavior, demonstrating that they can use odor plumes to find food. In a three-station discrimination task carried out in the dark, octopus showed a strong preference to move upstream towards the food-baited target, supporting the hypothesis that they are performing odor-guided search. When seeking a single baited target, also in the dark, octopuses not only preferred to move upstream towards the food source, but they also displayed characteristic motions associated with odor-gated rheotaxis, a commonly used odor tracking strategy used by many animals, which includes pausing, switchbacks, and across-stream redirections to the bait. Additionally, when approaching single baited stations the octopus often made reactive fast lunging motions. The observation of these fast arm-aligned motions (FAAM), taken together with the observation that the octopus did not have a characteristic body axis orientation to the bait, as would be expected if bilaterally symmetric organs such as the olfactory pits guided this behavior, supports the hypothesis that the suckers are the primary chemosensory organs driving octopus odor-guided behaviors.

animal behavior and cognition↗

bioRxiv2024

The spiking output of the mouse olfactory bulb encodes large-scale temporal features of natural odor environments

In natural odor environments, odor travels in plumes. Odor concentration dynamics change in characteristic ways across the width and length of a plume. Thus, spatiotemporal dynamics of plumes have informative features for animals navigating to an odor source. Population activity in the olfactory bulb (OB) has been shown to follow odor concentration across plumes to a moderate degree (Lewis et al., 2021). However, it is unknown whether the ability to follow plume dynamics is driven by individual cells or whether it emerges at the population level. Previous research has explored the responses of individual OB cells to isolated features of plumes, but it is difficult to adequately sample the full feature space of plumes as it is still undetermined which features navigating mice employ during olfactory guided search. Here we released odor from an upwind odor source and simultaneously recorded both odor concentration dynamics and cellular response dynamics in awake, head-fixed mice. We found that longer timescale features of odor concentration dynamics were encoded at both the cellular and population level. At the cellular level, responses were elicited at the beginning of the plume for each trial, signaling plume onset. Plumes with high odor concentration elicited responses at the end of the plume, signaling plume offset. Although cellular level tracking of plume dynamics was observed to be weak, we found that at the population level, OB activity distinguished whiffs and blanks (accurately detected odor presence versus absence) throughout the duration of a plume. Even [~]20 OB cells were enough to accurately discern odor presence throughout a plume. Our findings indicate that the full range of odor concentration dynamics and high frequency fluctuations are not encoded by OB spiking activity. Instead, relatively lower-frequency temporal features of plumes, such as plume onset, plume offset, whiffs, and blanks, are represented in the OB.

neuroscience↗

bioRxiv2023

Dynamics of odor-source localization: Insights from real-time odor plume recordings and head-motion tracking in freely moving mice

Animals navigating turbulent odor plumes exhibit a rich variety of behaviors, and employ efficient strategies to locate odor sources. A growing body of literature has started to probe this complex task of localizing airborne odor sources in walking mammals to further our understanding of neural encoding and decoding of naturalistic sensory stimuli. However, correlating the intermittent olfactory information with behavior has remained a long-standing challenge due to the stochastic nature of the odor stimulus. We recently reported a method to record real-time olfactory information available to freely moving mice during odor-guided navigation, hence overcoming that challenge. Here we combine our odor-recording method with head-motion tracking to establish correlations between plume encounters and head movements. We show that mice exhibit robust head-pitch motions in the 5-14Hz range during an odor-guided navigation task, and that these head motions are modulated by plume encounters. Furthermore, mice reduce their angles with respect to the source upon plume contact. Head motions may thus be an important part of the sensorimotor behavioral repertoire during naturalistic odor-source localization.

neuroscience↗

bioRxiv2023

Octopus arm search strategies over complex surfaces

Despite the extreme flexibility of the octopuss arms and their resulting near infinite possible configurations, the octopus effectively controls its arms during a wide variety of behaviors, including locomotion, foraging, excavation, exploration, and manipulation. If appropriately characterized, the octopuss biomechanical properties and control strategies could be implemented in the development of a soft robotic limb with the same range of capabilities. When operating without visual feedback, the octopus must rely on the complex chemotactile sensory system within its suckers, and in these conditions sucker recruitment plays a prominent role in search behavior, causing the arm to conform to surface features in the environment. However, how this mechanism is used to search over the complex and convoluted surfaces in the octopuss natural habitat is unknown. Here, we investigate the strategies the octopus uses to search for a reward hidden among a row of multiple small openings of a task space, and how it uses multiple arms to search three parallel versions of this task space. We found that when the arm encounters multiple openings in a surface, it performs a distal to proximal search pattern, starting with the farthest openings within reach then working its way proximally with a preference for searching each opening in succession. This strategy would allow the octopus to use its highly flexible limbs to perform an exhaustive search pattern over complex surfaces.

animal behavior and cognition↗

bioRxiv2023

Mechanisms of octopus arm search behavior without visual feedback

The octopus coordinates multiple, highly flexible arms with the support of a complex distributed nervous system. The octopuss suckers, staggered along each arm, are employed in a wide range of behaviors. Many of these behaviors, such as foraging in visually occluded spaces, are executed under conditions of limited or absent visual feedback. In coordinating unseen limbs with seemingly infinite degrees of freedom across a variety of adaptive behaviors, the octopus appears to have solved a significant control problem facing the field of soft-bodied robotics. To study the strategies that the octopus uses to find and capture prey within unseen spaces, we designed and 3D printed visually occluded foraging tasks and tracked arm motion as the octopus attempted to find and retrieve a food reward. By varying the location of the food reward within these tasks, we can characterize how the arms and suckers adapt to their environment to find and capture prey. We compared these results to simulated experimental conditions performed by a model octopus arm to isolate the primary mechanisms driving our experimental observations. We found that the octopus relies on a contact-based search strategy that emerges from local sucker coordination to simplify the control of its soft, highly flexible limbs.

animal behavior and cognition↗

bioRxiv2021

The lesser Pacific striped octopus, Octopus chierchiae: an emerging laboratory model for the study of octopuses

Cephalopods have the potential to become useful experimental models in various fields of science, particularly in neuroscience, physiology, and behavior. Their complex nervous systems, intricate color- and texture-changing body patterns, and problem-solving abilities have attracted the attention of the biological research community, while the high growth rates and short life cycles of some species render them suitable for laboratory culture. Octopus chierchiae is a small octopus native to the central Pacific coast of North America whose predictable reproduction, short time to maturity, small adult size, and ability to lay multiple egg clutches (iteroparity) make this species ideally suited to laboratory culture. Here we describe novel methods for culture of O. chierchiae, with emphasis on enclosure designs, feeding regimes, and breeding management. Our results demonstrate the feasibility of multigenerational culture of O. chierchiae. Specifically, O. chierchiae bred in the laboratory grows from a 3.5-millimeter mantle length at hatching to an adult mantle length of approximately 20-30 millimeters in 250-300 days, with 14-15% survivorship to over 400 days of age in first and second generations. O. chierchiae sexually matures at around an estimated six months of age and, unlike most octopus species, can lay multiple clutches of eggs, approximately every 30-90 days. Eggs are large and hatchlings emerge as direct developing octopuses. Based on these results, we propose that O. chierchiae possesses both the practical and biological features needed for a model octopus that can be cultured repeatedly to address a wide range of fundamental biological questions.

animal behavior and cognition↗

bioRxiv2021

A machine learning approach for detecting vicarious trial and error behaviors

Vicarious trial and error behaviors (VTEs) indicate periods of indecision during decision-making, and have been proposed as a behavioral marker of deliberation. In order to understand the neural underpinnings of these putative bridges between behavior and neural dynamics, researchers need the ability to readily distinguish VTEs from non-VTEs. Here we utilize a small set of trajectory-based features and standard machine learning classifiers to identify VTEs from non-VTEs for rats performing a spatial delayed alternation task (SDA) on an elevated plus maze. We also show that previously reported features of the hippocampal field potential oscillation can be used in the same types of classifiers to separate VTEs from non-VTEs with above chance performance. However, we caution that the modest classifier success using hippocampal population dynamics is not sufficient for identifying trials where VTEs occur, and show that combining oscillation-based features with trajectory-based features degrades classifier performance compared to trajectory-based features alone. Overall, we propose a standard set of features useful for trajectory-based VTE classification and support previous suggestions that VTEs are supported by a network including, but likely extending beyond, the hippocampus.

neuroscience↗

bioRxiv2020

Plume dynamics structure the spatiotemporal activity of glomerular networks in the mouse olfactory bulb

Although mice locate resources using turbulent airborne odor plumes, the stochasticity and intermittency of fluctuating plumes create challenges for interpreting odor cues in natural environments. Population activity within the olfactory bulb (OB), is thought to process this complex spatial and temporal information, but how plume dynamics impact odor representation in this early stage of the mouse olfactory system is not known. Limitations in odor detection technology have made it impossible to measure plume fluctuations while simultaneously recording from the mouses brain. Thus, previous studies have measured OB activity following controlled odor pulses of varying profiles or frequencies, but this approach only captures a subset of features found within olfactory plumes. Adequately sampling this feature space is difficult given a lack of knowledge regarding which features the brain extracts during exposure to natural olfactory scenes. Here we measured OB responses to naturally fluctuating odor plumes using a miniature, adapted odor sensor combined with wide-field GCaMP6f signaling from the dendrites of mitral and tufted (MT) cells imaged in olfactory glomeruli of head-fixed mice. We precisely tracked plume dynamics and imaged glomerular responses to this fluctuating input, while varying flow conditions across a range of ethologically-relevant values. We found that a consistent portion of MT activity in glomeruli follows odor concentration dynamics, and the strongest responding glomeruli are the best at following fluctuations within odor plumes. Further, the reliability and average response magnitude of glomerular populations of MT cells are affected by the flow condition in which the animal samples the plume, with the fidelity of plume following by MT cells increasing in conditions of higher flow velocity where odor dynamics result in intermittent whiffs of stronger concentration. Thus, the flow environment in which an animal encounters an odor has a large-scale impact on the temporal representation of an odor plume in the OB. Additionally, across flow conditions odor dynamics are a major driver of activity in many glomerular networks. Taken together, these data demonstrate that plume dynamics structure olfactory representations in the first stage of odor processing in the mouse olfactory system.

neuroscience↗

bioRxiv2019

Many paths to the same goal: metaheuristic operation of brains during natural behavior

During self-guided behaviors animals rapidly identify the constraints of the problems they face and adaptively employ appropriate cognitive strategies and heuristics to solve these problems1,2. This ability is currently an area of active investigation in artificial intelligence3. Recent work in computer science has suggested that this type of flexible problem solving could be achievable with metaheuristic approaches in which specific algorithms are selected based upon the identified demands of the problem to be solved4,5,6,7. Investigating how animals employ such metaheuristics while solving self-guided natural problems is a fertile area for biologically inspired algorithm development. Here we show that animals adaptively shift cognitive resources between sensory and memory systems during natural behavior to optimize performance under uncertainty. We demonstrate this using a new, laboratory-based discovery method to define the strategies used to solve a difficult optimization scenario, the stochastic \"traveling salesman\" problem5,8,9. Using this system we precisely manipulated the strength of prior information available to animals as well as the complexity of the problem. We find that rats are capable of efficiently solving this problem, even under conditions in which prior information is unreliable and the space of possible solutions is large. We compared animal performance to a Bayesian search and found that performance is consistent with a metaheuristic approach that adaptively allocates cognitive resources between sensory processing and memory, enhancing sensory acuity and reducing memory load under conditions in which prior information is unreliable. Our findings set the foundation for new approaches to understand the neural substrates of natural behavior as well as the rational development of biologically inspired metaheuristic approaches for complex real-world optimization.

animal behavior and cognition↗

bioRxiv2019

Using low-cost alcohol sensors to monitor real-time olfactory information during odor-guided navigation

Olfaction -- an evolutionarily conserved chemosensory modality -- guides navigation and decision-making in organisms from multiple phyla within the animal kingdom. However, using olfactory cues to guide navigation is a complicated problem. This is because the spread of odor molecules from the source is governed by turbulent and chaotic air currents, resulting in intermittent and spatiotemporally varying sensory cues as odor plumes. Precisely correlating olfactory information with behavior and neurophysiology from freely behaving animals has thus been a challenging avenue due to the dynamic nature of the odor plumes. Current technologies for chemical quantification are cumbersome and not feasible for monitoring the olfactory information at the temporal and spatial scales relevant for plume and odor tracking in animals. Here we present an alternate method for real-time monitoring of olfactory information using low-cost, lightweight sensors that robustly detect common solvent molecules, like alcohols. Paired recordings were made from these ethanol sensors with a Photoionization detector (PID) to precisely controlled ethanol stimuli. The ethanol sensor recordings were then deconvolved using a double exponential kernel, showing robust correlations with the PID recordings at behaviorally relevant time, frequency and spatial scales. Furthermore, the light weight of these sensors allows us to mount them on the heads of freely behaving rodents engaged in odor-guided navigation. Our preliminary experiments in mice show robust behavioral and neurophysiological responses correlated with ethanol plume contacts detected by these sensors.

neuroscience↗

bioRxiv2018

Thresholding of sensory inputs by extrasynaptic glutamate receptors in olfactory bulb glomeruli

The mammalian olfactory bulb has presented a challenging system for understanding information processing, in part because the bulb largely lacks the topographical ordering of neurons that promotes processes such as lateral inhibition. Here we have used dual and triple-cell recordings in rodent bulb slices combined with ultrastructural methods to provide the first experimental evidence for a processing mechanism circumventing this problem that operates at the level of single glomeruli, the bulbs odorant receptor-specific modules. A key feature is non-traditional, extrasynaptic glutamatergic signaling derived from excitatory interneurons and what it means for the local balance between excitation (E) and inhibition (I). We found that the distinct dynamic properties of extrasynaptic excitation versus synaptic inhibition create a thresholding effect whereby only strong stimuli produce a favorable E/I balance enabling an output. This single-glomerulus threshold could have a number of important functions during natural odor responses, for example enhancing stimulus tuning.

neuroscience↗