Biology subjects

Cleland, T. A.

Publications and source records attributed to Cleland, T. A..

6 recordsLinked to original sources

bioRxiv2022

EVIDENCE FOR EMPATHY IN PAIR BONDING POISON FROGS

More than a century ago, Charles Darwin hypothesized that the empathy-like phenotype is a phylogenetically widespread phenomenon. This idea remains contentious, due to the challenges of empirically examining emotions, and few investigations among non-mammalian vertebrates. We provide support for Darwins hypothesis by discovering partial evidence for the most ancestral form of empathy, emotional contagion (i.e., matching another individuals emotional state), in the pair bonding mimetic poison frog, Ranitomeya imitator. We found that male corticosterone, a physiological biomarker of stress, positively correlates with female partners in experimental and semi-natural conditions. This does not appear to coincide with behavioral state-matching. However, it is specific to female partners relative to familiar female non-partners, and is independent of effects that commonly confound studies on emotional contagion. Furthermore, this physiological state-matching is irrespective of partnership longevity or lifetime reproductive output. These results physiologically indicate socially selective emotional contagion in a monogamous amphibian, and paradigms that elicit coinciding neural and behavioral indicators and morphogenic co-variation are needed for further corroboration. Further studies on ancestral forms of empathy in non-mammalian vertebrates are warranted.

animal behavior and cognition↗

bioRxiv2022

Rates but not acoustic features of ultrasonic vocalizations are related to non-vocal behaviors in mouse pups

Mouse pups produce ultrasonic vocalizations (USVs) in response to isolation from the nest (i.e., isolation USVs). Rates and acoustic features of isolation USVs change dramatically over the first two weeks of life, and there is also substantial variability in the rates and acoustic features of isolation USVs at a given postnatal age. The factors that contribute to within-age variability in isolation USVs remain largely unknown. Here, we explore the extent to which non-vocal behaviors of mouse pups relate to the within-age variability in rates and acoustic features of their USVs. We recorded non-vocal behaviors of isolated C57BL/6J mouse pups at four postnatal ages (postnatal days 5, 10, 15, and 20), measured rates of isolation USV production, and applied a combination of hand-picked acoustic feature measurements and an unsupervised machine learning-based vocal analysis method to examine USV acoustic features. When we considered different categories of non-vocal behavior, our analyses revealed that mice in all postnatal age groups produce higher rates of isolation USVs during active non-vocal behaviors than when lying still. Moreover, rates of isolation USVs are correlated with the intensity (i.e., magnitude) of non-vocal body and limb movements within a given trial. In contrast, USVs produced during different categories of non-vocal behaviors and during different intensities of non-vocal movement do not differ substantially in their acoustic features. Our findings suggest that levels of behavioral arousal contribute to within-age variability in rates, but not acoustic features, of mouse isolation USVs.

animal behavior and cognition↗

bioRxiv2022

Dynamics of spike time encoding in the olfactory bulb

In the mammalian olfactory bulb (OB), gamma oscillations in the local field potential are generated endogenously during odor sampling. Such oscillations arise from dynamical systems that generate organized periodic behavior in neural circuits, and correspond to spike timing constraints at fine timescales. While the cellular and network mechanisms of gamma oscillogenesis in the OB are reasonably well established, it remains unclear how these fine-timescale dynamics serve to represent odors. Are patterns of spike synchrony on the gamma timescale replicable and odor-specific? Does the transformation to a spike-timing metric embed additional computations? To address these questions, we used OB slices to examine the spike timing dynamics evoked by "fictive odorants" generated via spatiotemporally patterned optogenetic stimulation of olfactory sensory neuron axonal arbors. We found that a small proportion of mitral/tufted cells phase-lock strongly to the fast oscillations evoked by fictive odorants, and exhibit tightly coupled spike-spike synchrony on the gamma timescale during this stimulation. Moreover, the specific population of synchronized neurons differed based on the "quality", but not the "concentration", of the fictive odorant presented, and was conserved across multiple presentations of the same fictive odorant. Given the established selectivity of piriform cortical pyramidal neurons for inputs synchronized on this timescale, we conclude that spike synchronization on a milliseconds timescale is a metric by which the OB encodes and exports afferent odor information in a concentration-invariant manner. As a corollary, mitral/tufted cell spikes that are not organized in time may not contribute effectively to the ensemble odor representation.

neuroscience↗

bioRxiv2020

A physicochemical model of odor sampling

We present a general physicochemical sampling model for olfaction, based on established pharmacological laws, in which arbitrary combinations of odorant ligands and receptors can be generated and their individual and collective effects on odor representations and olfactory performance measured. Individual odor ligands exhibit receptor-specific affinities and efficacies; that is, they may bind strongly or weakly to a given receptor, and can act as strong agonists, weak agonists, partial agonists, or antagonists. Ligands interacting with common receptors compete with one another for dwell time; these competitive interactions appropriately simulate the degeneracy that fundamentally defines the capacities and limitations of odorant sampling. The outcome of these competing ligand-receptor interactions yields a pattern of receptor activation levels, thereafter mapped to glomerular presynaptic activation levels based on the convergence of sensory neuron axons. The metric of greatest interest is the mean discrimination sensitivity, a measure of how effectively the olfactory system at this level is able to recognize a small change in the physicochemical quality of a stimulus. This model presents several significant outcomes, both expected and surprising. First, adding additional receptors reliably improves the systems discrimination sensitivity. Second, in contrast, adding additional ligands to an odor scene initially can improve discrimination sensitivity, but eventually will reduce it as the number of ligands increases. Third, the presence of antagonistic ligand-receptor interactions produced clear benefits for sensory system performance, generating higher absolute discrimination sensitivities and increasing the numbers of competing ligands that could be present before discrimination sensitivity began to be impaired. Finally, the model correctly reflects and explains the modest reduction in odor discrimination sensitivity exhibited by transgenic mice in which the specificity of glomerular targeting by primary olfactory neurons is partially disrupted. Author SummaryWe understand most sensory systems by comparing the responses of the system against objective external physical measurements. For example, we know that our ability to distinguish small changes in color is greater for some colors than for others, and that we can distinguish sounds more acutely when they are within the range of pitches used for speech. Similar principles presumably apply to the sense of smell, but odorous chemicals are harder to physically quantify than light or sound because they cannot be organized in terms of a straightforward physical variable like wavelength or frequency. That said, the physical properties of interactions between chemicals and cellular receptors (such as those in the olfactory system) are well understood. What we lack is a systematic framework within which these pharmacological principles can be organized to study odor sampling in the way that we have long studied visual and auditory sampling. We here propose and describe such a framework for odor sampling, and show that it successfully replicates some established but unexplained experimental results.

neuroscience↗

bioRxiv2020

Context-dependent odor learning requires the anterior olfactory nucleus

Learning to associate the context in which a stimulus occurs is an important aspect of animal learning. We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampal networks (vHC) to the anterior olfactory nucleus (AON). Using a contextually-cued olfactory discrimination task, rats were trained to associate two olfactory stimuli with different responses depending on visuo-spatial context. Temporary lesions of the AON or vHC impaired performance on this task. In contrast, such lesions did not impair performance on a non-contextual olfactory discrimination task. Moreover, vHC lesions also impaired performance on an analogous contextually-cued texture discrimination task, whereas AON lesions affected only olfactory contextual associations. We describe a distinct role for the AON in olfactory processing, and conclude that early olfactory networks such as the olfactory bulb and AON function as multimodal integration networks rather than processing olfactory signals exclusively. Significance statementContextual information has long been known to play a key role in cognitive functions such as memory and decision making. We here show the contextual modulation of neural information in early primary sensory networks and its effects on contextually conditional learned behavior. We propose that projections from ventral hippocampus to anterior olfactory nucleus convey contextual information to the early olfactory system, modulating sensory representations and olfactory perception. Using behavioral pharmacology and computational modeling, we show how established network structures can mediate multimodal information and use context to make olfactory decisions.

neuroscience↗

bioRxiv2017

Coherent olfactory bulb gamma oscillations arise from coupling independent columnar oscillators

Spike timing-based representations of sensory information depend on embedded dynamical frameworks within neuronal networks that establish the rules of local computation and interareal communication. Here, we investigated the dynamical properties of olfactory bulb circuitry in mice of both sexes using microelectrode array recordings from slice and in vivo preparations. Neurochemical activation or optogenetic stimulation of sensory afferents evoked persistent gamma oscillations in the local field potential. These oscillations arose from slower, GABA(A) receptor-independent intracolumnar oscillators coupled by GABA(A)-ergic synapses into a faster, broadly coherent network oscillation. Consistent with the theoretical properties of coupled-oscillator networks, the spatial extent of zero-phase coherence was bounded in slices by the reduced density of lateral interactions. The intact in vivo network, however, exhibited long-range lateral interactions that suffice in simulation to enable zero-phase gamma coherence across the olfactory bulb. The timing of action potentials in a subset of principal neurons was phase-constrained with respect to evoked gamma oscillations. Coupled-oscillator dynamics in olfactory bulb thereby enable a common clock, robust to biological heterogeneities, that is capable of supporting gamma-band spike synchronization and phase coding across the ensemble of activated principal neurons. New & NoteworthyOdor stimulation evokes rhythmic gamma oscillations in the field potential of the olfactory bulb, but the dynamical mechanisms governing these oscillations have remained unclear. Establishing these mechanisms is important, as they determine the biophysical capacities of the bulbar circuit to, for example, maintain zero-phase coherence across a spatially extended network, or coordinate the timing of action potentials in principal neurons. These properties in turn constrain and suggest hypotheses of sensory coding.

neuroscience↗