Traditional rodent models of Pavlovian fear conditioning assess the strength of learning by quantifying freezing responses. However, sole reliance on this measure includes the de facto assumption that any locomotor activity reflects an absence of fear. Consequently, alternative expressions of associative learning are rarely considered. Here we identify a novel, active fear response (‘darting’) that occurs primarily in female rats. In females, darting exhibits the characteristics of a learned fear behavior, appearing during the CS period as conditioning proceeds and disappearing from the CS period during extinction. This finding motivates a reinterpretation of rodent fear conditioning studies, particularly in females, and it suggests that conditioned fear behavior is more diverse than previously appreciated. Moreover, rats that darted during initial fear conditioning exhibited lower freezing during the second day of extinction testing, suggesting that females employ distinct and adaptive fear response strategies that improve long-term outcomes.DOI: http://dx.doi.org/10.7554/eLife.11352.001

Neurodevelopmental disorders are marked by inappropriate synaptic connectivity early in life, but how disruption of experience-dependent plasticity contributes to cognitive and behavioural decline in adulthood is unclear. Here we show that pup gathering behaviour and associated auditory cortical plasticity are impaired in female Mecp2het mice, a model of Rett syndrome. In response to learned maternal experience, Mecp2het females exhibited transient changes to cortical inhibitory networks typically associated with limited plasticity. Averting these changes in Mecp2het through genetic or pharmacological manipulations targeting the GABAergic network restored gathering behaviour. We propose that pup gathering learning triggers a transient epoch of inhibitory plasticity in auditory cortex that is dysregulated in Mecp2het. In this window of heightened sensitivity to sensory and social cues, Mecp2 mutations suppress adult plasticity independently from their effects on early development.

Natural odorants are complex mixtures of diverse chemical compounds. Monomolecular odorants are represented in the main olfactory bulb by distinct spatial patterns of activated glomeruli. However, it remains unclear how individual compounds contribute to population representations of natural stimuli, which appear to be unexpectedly sparse. We combined gas chromatography and intrinsic signal imaging to visualize glomerular responses to natural stimuli and their fractionated components. While whole stimuli activated up to 20 visible glomeruli, each fractionated component activated only one or few glomeruli, and most glomeruli were activated by only one component. Thus, responses to complex mixtures reflected activation by multiple components, with each contributing only a small part of the overall representation. We conclude that the population response to a complex stimulus is largely the sum of the responses to its individual components, and activation of an individual glomerulus independently signals the presence of a specific component.

Sensory systems may adapt to behavioral requirements through state-dependent changes. In the forebrain song-system nucleus HVc of zebra finches, state-dependent auditory responses have been described in multiunit recordings. Here we report on behavioral state-dependent changes in the activity of distinct HVc neuronal classes. HVc projection neurons were identified by electrically stimulating HVc's target nuclei, the robust nucleus of the archistriatum and Area X, in anesthetized zebra finches. Projection neurons and two classes of putative interneurons could be distinguished on the basis of extracellular spike waveforms, with the first two factors of a principal components analysis accounting for 81% of the variance in spike morphometric values. Spike width was the best single variable for distinguishing among the neuronal classes. Putative interneurons had much higher firing rates spontaneously and in response to song than did projection neurons, which had extremely low spontaneous rates and phasic responses to song. Recordings from HVc in behaving animals were dominated by the two classes of putative interneurons. Both classes showed strong, selective, and temporally similar auditory responses during sleep, but only one class of interneurons reliably maintained auditory responses on waking. These responses were weaker and less selective than those seen during sleep. The observation that HVc auditory responsiveness in awake zebra finches is restricted to some classes of neurons may help explain prior multiunit results that suggested nearly complete suppression of HVc auditory responses in awake birds. We propose that the heterogeneous effects of behavioral state on distinct subpopulations of HVc neurons allow HVc to participate in multiple roles during song production, conspecific song recognition, and possibly memory consolidation during sleep.

Budgerigars throughout life are capable of learning to produce many different sounds including those of human speech. Like humans, budgerigars use multiple craniomotor systems and coordinate both orosensory and auditory feedback in specialized forebrain nuclei. Although budgerigar auditory-vocal learning has a different evolutionary origin from that of human speech, both the human and budgerigar systems can control F0 and can alter the distribution of energy in spectral bands by adjusting the filter properties of the vocal tract. This allows budgerigars to produce an extremely diverse array of calls including many broadband and highly complex sounds.

No abstract

For many mammals, individual recognition of conspecifics relies on olfactory cues. Certain individual recognition memories are thought to be stored when conspecific odor cues coincide with surges of noradrenaline (NA) triggered by intensely arousing social events. Such familiar stimuli elicit reduced behavioral responses, a change likely related to NA-dependent plasticity in the olfactory bulb (OB). In addition to its role in these ethological memories, NA signaling in the OB appears to be relevant for the discrimination of more arbitrary odorants as well. Nonetheless, no NA-gated mechanism of long-term plasticity in the OB has ever been directly observed in vivo. Here, we report that NA release from locus ceruleus (LC), when coupled to odor presentation, acts locally in the main OB to cause a specific long-lasting suppression of responses to paired odors. These effects were observed for both food odors and urine, an important social recognition cue. Moreover, in subsequent behavioral tests, mice exhibited habituation to paired urine stimuli, suggesting that this LC-mediated olfactory neural plasticity, induced under anesthesia, can store an individual recognition memory that is observable after recovery.

Olfactory representations are shaped by brain state and respiration. The interaction and circuit substrates of these influences are unclear. Granule cells (GCs) in the main olfactory bulb (MOB) are presumed to sculpt activity reaching the cortex via inhibition of mitral/tufted cells (MTs). GCs potentially make ensemble activity more sparse by facilitating lateral inhibition among MTs and/or enforce temporally precise activity locked to breathing. Yet the selectivity and temporal structure of wakeful GC activity are unknown. We recorded GCs in the MOB of anesthetized and awake mice and identified state-dependent features of odor coding and temporal patterning. Under anesthesia, GCs were sparsely active and strongly and synchronously coupled to respiration. Upon waking, GCs desynchronized, broadened their tuning and largely fired independently from respiration. Thus, during wakefulness, GCs exhibited stronger odor responses with less temporal structure. We propose that during wakefulness GCs may shape MT odor responses through broadened lateral interactions rather than respiratory synchronization.