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1.
PLoS Biol ; 20(11): e3001896, 2022 11.
Article in English | MEDLINE | ID: mdl-36441759

ABSTRACT

Higher-order sensory thalamic nuclei are densely connected with multiple cortical and subcortical areas, yet the role of these nuclei remains elusive. The posteromedial thalamic nucleus (POm), the higher-order thalamic nucleus in the rodent somatosensory system, is an anatomical hub broadly connected with multiple sensory and motor brain areas yet weakly responds to passive sensory stimulation and whisker movements. To understand the role of POm in sensory perception, we developed a self-initiated, two-alternative forced-choice task in freely moving mice during active sensing. Using optogenetic and chemogenetic manipulation, we show that POm plays a significant role in sensory perception and the projection from the primary somatosensory cortex to POm is critical for the contribution of POm in sensory perception during active sensing.


Subject(s)
Thalamic Nuclei , Animals , Mice
2.
J Neurosci ; 35(5): 1965-78, 2015 Feb 04.
Article in English | MEDLINE | ID: mdl-25653355

ABSTRACT

Systemic administration of cocaine is thought to decrease the firing rates of ventral tegmental area (VTA) dopamine (DA) neurons. However, this view is based on categorizations of recorded neurons as DA neurons using preselected electrophysiological characteristics lacking neurochemical confirmation. Without applying cellular preselection, we recorded the impulse activity of VTA neurons in response to cocaine administration in anesthetized adult rats. The phenotype of recorded neurons was determined by their juxtacellular labeling and immunohistochemical detection of tyrosine hydroxylase (TH), a DA marker. We found that intravenous cocaine altered firing rates in the majority of recorded VTA neurons. Within the cocaine-responsive neurons, half of the population was excited and the other half was inhibited. Both populations had similar discharge rates and firing regularities, and most neurons did not exhibit changes in burst firing. Inhibited neurons were more abundant in the posterior VTA, whereas excited neurons were distributed evenly throughout the VTA. Cocaine-excited neurons were more likely to be excited by footshock. Within the subpopulation of TH-positive neurons, 36% were excited by cocaine and 64% were inhibited. Within the subpopulation of TH-negative neurons, 44% were excited and 28% were inhibited. Contrary to the prevailing view that all DA neurons are inhibited by cocaine, we found a subset of confirmed VTA DA neurons that is excited by systemic administration of cocaine. We provide evidence indicating that DA neurons are heterogeneous in their response to cocaine and that VTA non-DA neurons play an active role in processing systemic cocaine.


Subject(s)
Action Potentials , Cocaine/pharmacology , Dopaminergic Neurons/drug effects , Ventral Tegmental Area/physiology , Administration, Intravenous , Animals , Cocaine/administration & dosage , Dopaminergic Neurons/physiology , Male , Neural Inhibition , Organ Specificity , Rats , Rats, Long-Evans , Ventral Tegmental Area/cytology , Ventral Tegmental Area/drug effects
3.
J Neurosci ; 34(8): 2940-55, 2014 Feb 19.
Article in English | MEDLINE | ID: mdl-24553935

ABSTRACT

Classical studies on the development of ocular dominance (OD) organization in primary visual cortex (V1) have revealed a postnatal critical period (CP), during which visual inputs between the two eyes are most effective in shaping cortical circuits through synaptic competition. A brief closure of one eye during CP caused a pronounced shift of response preference of V1 neurons toward the open eye, a form of CP plasticity in the developing V1. However, it remains unclear what particular property of binocular inputs during CP is responsible for mediating this experience-dependent OD plasticity. Using whole-cell recording in mouse V1, we found that visually driven synaptic inputs from the two eyes to binocular cells in layers 2/3 and 4 became highly coincident during CP. Enhancing cortical GABAergic transmission activity by brain infusion with diazepam not only caused a precocious onset of the high coincidence of binocular inputs and OD plasticity in pre-CP mice, but rescued both of them in dark-reared mice, suggesting a tight link between coincident binocular inputs and CP plasticity. In Thy1-ChR2 mice, chronic disruption of this binocular input coincidence during CP by asynchronous optogenetic activation of retinal ganglion cells abolished the OD plasticity. Computational simulation using a feed-forward network model further suggests that the coincident inputs could mediate this CP plasticity through a homeostatic synaptic learning mechanism with synaptic competition. These results suggest that the high-level correlation of binocular inputs is a hallmark of the CP of developing V1 and serves as neural substrate for the induction of OD plasticity.


Subject(s)
Critical Period, Psychological , Dominance, Ocular/physiology , Neuronal Plasticity/physiology , Vision, Binocular/physiology , Visual Cortex/physiology , Animals , Channelrhodopsins , Computer Simulation , Female , Immunohistochemistry , Male , Mice , Mice, Inbred C57BL , Mice, Transgenic , Models, Neurological , Optogenetics , Patch-Clamp Techniques , Photic Stimulation , Retinal Ganglion Cells/physiology , Synapses/physiology , Visual Cortex/growth & development , Visual Fields/physiology , gamma-Aminobutyric Acid/physiology
4.
J Neurosci ; 30(5): 1861-8, 2010 Feb 03.
Article in English | MEDLINE | ID: mdl-20130195

ABSTRACT

Frequency modulation (FM) is a prominent feature in animal vocalization and human speech. Although many neurons in the auditory cortex are known to be selective for FM direction, the synaptic mechanisms underlying this selectivity are not well understood. Previous studies of both visual and auditory neurons have suggested two general mechanisms for direction selectivity: (1) differential delays of excitatory inputs across the spatial/spectral receptive field and (2) spatial/spectral offset between excitatory and inhibitory inputs. In this study, we have examined the contributions of both mechanisms to FM direction selectivity in rat primary auditory cortex. The excitatory and inhibitory synaptic inputs to each cortical neuron were measured by in vivo whole-cell recording. The spectrotemporal receptive field of each type of inputs was mapped with random tone pips and compared with direction selectivity of the neuron measured with FM stimuli. We found that both the differential delay of the excitatory input and the spectral offset between excitation and inhibition are positively correlated with direction selectivity of the neuron. Thus, both synaptic mechanisms are likely to contribute to FM direction selectivity in the auditory cortex. Finally, direction selectivity measured from the spiking output is significantly stronger than that based on the subthreshold membrane potentials, indicating that the selectivity is further sharpened by the spike generation mechanism.


Subject(s)
Auditory Cortex/physiology , Sound Localization/physiology , Synapses/physiology , Action Potentials , Animals , Brain Mapping , Male , Membrane Potentials , Models, Neurological , Patch-Clamp Techniques , Pitch Perception/physiology , Rats , Rats, Sprague-Dawley , Reaction Time
5.
J Neurosci ; 29(18): 6013-21, 2009 May 06.
Article in English | MEDLINE | ID: mdl-19420268

ABSTRACT

Slow oscillations at frequencies <1 Hz manifest in many brain regions as discrete transitions between a depolarized up state and a hyperpolarized down state of the neuronal membrane potential. Although up and down states are known to differentially affect sensory-evoked responses, whether and how they are modulated by sensory stimuli are not well understood. In the present study, intracellular recording in anesthetized guinea pigs showed that membrane potentials of nonlemniscal auditory thalamic neurons exhibited spontaneous up/down transitions at random intervals in the range of 2-30 s, which could be entrained to a regular interval by repetitive sound stimuli. After termination of the entraining stimulation (ES), regular up/down transitions persisted for several cycles at the ES interval. Furthermore, the efficacy of weak sound stimuli in triggering the up-to-down transition was potentiated specifically at the ES interval for at least 10 min. Extracellular recordings in the auditory thalamus of unanesthetized guinea pigs also showed entrainment of slow oscillations by rhythmic sound stimuli during slow wave sleep. These results demonstrate a novel form of network plasticity, which could help to retain the information of stimulus interval on the order of seconds.


Subject(s)
Membrane Potentials/physiology , Periodicity , Sensory Receptor Cells/physiology , Sound , Thalamus/cytology , Acoustic Stimulation/methods , Action Potentials/physiology , Animals , Guinea Pigs , Psychoacoustics , Spectrum Analysis , Time Factors , Wakefulness
6.
J Neurosci ; 26(11): 3002-9, 2006 Mar 15.
Article in English | MEDLINE | ID: mdl-16540578

ABSTRACT

Two major aspects of dendritic integration, coincidence detection and temporal integration, depend critically on the spatial and temporal properties of the dendritic summation of synaptic inputs. Neuronal activity capable of inducing synaptic long-term potentiation (LTP) leads to increased linearity of the spatial summation of synchronous EPSPs. Whether such activity can also modulate the temporal summation of EPSPs is unknown. In the present study, we examined the linearity of the summation of EPSPs spaced by different time intervals in hippocampal CA1 pyramidal neurons, before and after LTP induction. We found that LTP induction resulted in an increased linearity of summation of the potentiated input with another synchronous or asynchronous input, with a striking dendritic location-specific selectivity for the timing of the summed inputs. At distal dendrites, LTP induction led to an increased linearity of summation only for EPSPs arriving within 5 ms, thus favoring the summation of coincident inputs. In contrast, LTP induction at proximal dendrites increased the linearity of summation for EPSPs arriving within a time window of >20 ms. Furthermore, for synaptic inputs at the distal dendrite, enhanced spiking output after LTP induction was observed only for coincidently summed EPSPs, suggesting facilitated coincidence detection. In contrast, for proximal inputs, enhanced spiking output after LTP induction occurred for EPSPs arriving within a broader time window of approximately 20 ms, favoring temporal integration. Such dendritic location-dependent differential modulation of coincidence detection and temporal integration by neuronal activity represents a form of activity-dependent and domain-specific plasticity in the function of dendritic information processing.


Subject(s)
Dendrites/physiology , Excitatory Postsynaptic Potentials/physiology , Long-Term Potentiation/physiology , Synaptic Transmission/physiology , Action Potentials/physiology , Animals , Hippocampus/cytology , Patch-Clamp Techniques , Rats , Rats, Sprague-Dawley , Time Factors
7.
Neuron ; 40(5): 971-82, 2003 Dec 04.
Article in English | MEDLINE | ID: mdl-14659095

ABSTRACT

Extracellular ATP released from axons is known to assist activity-dependent signaling between neurons and Schwann cells in the peripheral nervous system. Here we report that ATP released from astrocytes as a result of neuronal activity can also modulate central synaptic transmission. In cultures of hippocampal neurons, endogenously released ATP tonically suppresses glutamatergic synapses via presynaptic P2Y receptors, an effect that depends on the presence of cocultured astrocytes. Glutamate release accompanying neuronal activity also activates non-NMDA receptors of nearby astrocytes and triggers ATP release from these cells, which in turn causes homo- and heterosynaptic suppression. In CA1 pyramidal neurons of hippocampal slices, a similar synaptic suppression was also produced by adenosine, an immediate degradation product of ATP released by glial cells. Thus, neuron-glia crosstalk may participate in activity-dependent synaptic modulation.


Subject(s)
Adenosine Triphosphate/metabolism , Astrocytes/metabolism , Glutamic Acid/metabolism , Neural Inhibition/physiology , Synapses/metabolism , Action Potentials/physiology , Adenosine Triphosphate/physiology , Animals , Astrocytes/physiology , Cells, Cultured , Hippocampus/metabolism , Rats , Rats, Sprague-Dawley , Synaptic Transmission/physiology
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