0000000000288350
AUTHOR
Maik C. Stüttgen
Temporally precise control of single-neuron spiking by juxtacellular nanostimulation
Temporal patterns of action potentials influence a variety of activity-dependent intra- and intercellular processes and play an important role in theories of neural coding. Elucidating the mechanisms underlying these phenomena requires imposing spike trains with precisely defined patterns, but this has been challenging due to the limitations of existing stimulation techniques. Here we present a new nanostimulation method providing control over the action potential output of individual cortical neurons. Spikes are elicited through the juxtacellular application of short-duration fluctuating currents (“kurzpulses”), allowing for the sub-millisecond precise and reproducible induction of arbitr…
Neurons in the pigeon caudolateral nidopallium differentiate Pavlovian conditioned stimuli but not their associated reward value in a sign-tracking paradigm
AbstractAnimals exploit visual information to identify objects, form stimulus-reward associations, and prepare appropriate behavioral responses. The nidopallium caudolaterale (NCL), an associative region of the avian endbrain, contains neurons exhibiting prominent response modulation during presentation of reward-predicting visual stimuli, but it is unclear whether neural activity represents valuation signals, stimulus properties, or sensorimotor contingencies. To test the hypothesis that NCL neurons represent stimulus value, we subjected pigeons to a Pavlovian sign-tracking paradigm in which visual cues predicted rewards differing in magnitude (large vs. small) and delay to presentation (s…
Barrel cortex: What is it good for?
The rodent whisker system, with barrel cortex as its most prominent structure, has evolved into a powerful model system to study sensory processing. However, despite the vast amount of data collected on barrel cortex neural activity patterns, as well as its circuitry and plasticity, the precise behavioral and cognitive operations for which this structure is needed are still elusive. Proposed functions of barrel cortex include detection, discrimination, coordination of whisker movements during exploratory locomotion or active touch, and associative learning. Departing from a definition of what exactly constitutes a function and how the involvement of a brain area in a specific task can be es…
Auditory cortex reflects goal-directed movement but is not necessary for behavioral adaptation in sound-cued reward tracking
Mounting evidence suggests that the role of sensory cortices in perceptual decision making goes beyond the mere representation of the discriminative stimuli and additionally involves the representation of nonsensory variables such as reward expectation. However, the relevance of these representations for behavior is not clear. To address this issue, we trained rats to discriminate sounds in a single-interval forced-choice task and then confronted the animals with unsignaled blockwise changes of reward probabilities. We found that unequal reward probabilities for the two choice options led to substantial shifts in response bias without concomitant reduction in stimulus discrimination. Althou…
Blocking NMDA-receptors in the pigeon's "prefrontal" caudal nidopallium impairs appetitive extinction learning in a sign-tracking paradigm
Extinction learning provides the ability to flexibly adapt to new contingencies by learning to inhibit previously acquired associations in a context-dependent manner. The neural networks underlying extinction learning were mostly studied in rodents using fear extinction paradigms. To uncover invariant properties of the neural basis of extinction learning, we employ pigeons as a model system. Since the prefrontal cortex of mammals is a key structure for extinction learning, we assessed the role of N-methyl-D-aspartate receptors (NMDARs) in the nidopallium caudolaterale, the avian functional equivalent of mammalian prefrontal cortex. Since NMDARs in prefrontal cortex have been shown to be rel…
Assessing the Impact of Single-Cell Stimulation on Local Networks in Rat Barrel Cortex—A Feasibility Study
In contrast to the long-standing notion that the role of individual neurons in population activity is vanishingly small, recent studies have shown that electrical activation of only a single cortical neuron can have measurable effects on global brain state, movement, and perception. Although highly important for understanding how neuronal activity in cortex is orchestrated, the cellular and network mechanisms underlying this phenomenon are unresolved. Here, we first briefly review the current state of knowledge regarding the phenomenon of single-cell induced network modulation and discuss possible underpinnings. Secondly, we show proof of principle for an experimental approach to elucidate …
Context specificity of both acquisition and extinction of a Pavlovian conditioned response
It is widely held that the extinction of a conditioned response is more context specific than its initial acquisition. One proposed explanation is that context serves to disambiguate the meaning of a stimulus. Using a procedure that equated the learning histories of the contexts, we show that the memory of an appetitive Pavlovian association can be highly context specific despite being unambiguous. This result is inconsistent with predictions of the Rescorla–Wagner model of learning but in line with configural accounts of contextual control of behavior. We propose an explanatory model in which context serves to modulate the gain of associative strength and which expands upon the configural …
Beyond the classic extinction network: a wider, comparative view
Abstract Extinction learning modifies the dynamics of brain circuits such that a previously learned conditioned response is no longer generated. The majority of extinction studies use fear conditioning in rodents and identified the prefrontal cortex, the hippocampus, and the amygdala as core regions of the extinction circuit. We sought to find answers to two questions: First, do we find a similar functional brain circuit in birds, which underwent a 300-million-year separate evolution from mammals? Second, do we have to incorporate the cerebellum as a key component of the central extinction circuit? We indeed show that the avian extinction pathways are not identical but highly similar to tho…
Temporal refinement of sensory-evoked activity across layers in developing mouse barrel cortex.
Rhythmic whisking behavior in rodents fully develops during a critical period about 2 weeks after birth, in parallel with the maturation of other sensory modalities and the onset of exploratory locomotion. How whisker-related sensory processing develops during this period in the primary somatosensory cortex (S1) remains poorly understood. Here, we characterized neuronal activity evoked by single- or dual-whisker stimulation patterns in developing S1, before, during and after the occurrence of active whisking. Employing multi-electrode recordings in all layers of barrel cortex in urethane-anesthetized mice, we find layer-specific changes in multi-unit activity for principal and neighboring b…
Optogenetic Modulation of a Minor Fraction of Parvalbumin-Positive Interneurons Specifically Affects Spatiotemporal Dynamics of Spontaneous and Sensory-Evoked Activity in Mouse Somatosensory Cortex in Vivo
Abstract Parvalbumin (PV) positive interneurons exert strong effects on the neocortical excitatory network, but it remains unclear how they impact the spatiotemporal dynamics of sensory processing in the somatosensory cortex. Here, we characterized the effects of optogenetic inhibition and activation of PV interneurons on spontaneous and sensory-evoked activity in mouse barrel cortex in vivo. Inhibiting PV interneurons led to a broad-spectrum power increase both in spontaneous and sensory-evoked activity. Whisker-evoked responses were significantly increased within 20 ms after stimulus onset during inhibition of PV interneurons, demonstrating high temporal precision of PV-shaped inhibition.…
Layer-Specific Refinement of Sensory Coding in Developing Mouse Barrel Cortex
Rodent rhythmic whisking behavior matures during a critical period around 2 weeks after birth. The functional adaptations of neocortical circuitry during this developmental period remain poorly understood. Here, we characterized stimulus-evoked neuronal activity across all layers of mouse barrel cortex before, during, and after the onset of whisking behavior. Employing multi-electrode recordings and 2-photon calcium imaging in anesthetized mice, we tested responses to rostro-caudal whisker deflections, axial "tapping" stimuli, and their combination from postnatal day 10 (P10) to P28. Within this period, whisker-evoked activity of neurons displayed a general decrease in layer 2/3 (L2/3) and …
Development of the whisker-to-barrel cortex system.
This review provides an overview on the development of the rodent whisker-to-barrel cortex system from late embryonic stage to the end of the first postnatal month. During this period the system shows a remarkable transition from a mostly genetic-molecular driven generation of crude connectivity, providing the template for activity-dependent structural and functional maturation and plasticity, to the manifestation of a complex behavioral repertoire including social interactions. Spontaneous and sensory-evoked activity is present in neonatal barrel cortex and control the generation of the cortical architecture. Half a century after its first description by Woolsey and van der Loos the whiske…
Neurons in the pigeon nidopallium caudolaterale signal the selection and execution of perceptual decisions
Sensory systems provide organisms with information on the current status of the environment, thus enabling adaptive behavior. The neural mechanisms by which sensory information is exploited for action selection are typically studied with mammalian subjects performing perceptual decision-making tasks, and most of what is known about these mechanisms at the single-neuron level is derived from cortical recordings in behaving monkeys. To explore the generality of neural mechanisms underlying perceptual decision making across species, we recorded single-neuron activity in the pigeon nidopallium caudolaterale (NCL), a non-laminated associative forebrain structure thought to be functionally equiva…