Proper neuronal function and several forms of synaptic plasticity are highly dependent on precise control of mRNA translation, particularly in dendrites. We find that eIF4AIII, a core exon junction complex (EJC) component loaded onto mRNAs by pre-mRNA splicing, is associated with neuronal mRNA granules and dendritic mRNAs. eIF4AIII knockdown markedly increases both synaptic strength and GLUR1 AMPA receptor abundance at synapses. eIF4AIII depletion also increases ARC, a protein required for maintenance of long-term potentiation; arc mRNA, one of the most abundant in dendrites, is a natural target for nonsense-mediated decay (NMD). Numerous new NMD candidates, some with potential to affect synaptic activity, were also identified computationally. Two models are presented for how translation-dependent decay pathways such as NMD might advantageously function as critical brakes for protein synthesis in cells such as neurons that are highly dependent on spatially and temporally restricted protein expression.
Learning tasks are typically thought to be either hippocampal-dependent (impaired by hippocampal lesions) or hippocampal-independent (indifferent to hippocampal lesions). Here, we show that conditioned taste aversion (CTA) learning fits into neither of these categories. Rats were trained to avoid two taste stimuli, one novel and one familiar. Muscimol infused through surgically implanted intracranial cannulae temporarily inactivated the dorsal hippocampus during familiarization, subsequent CTA training, or both. As shown previously, hippocampal inactivation during familiarization enhanced the effect of that familiarization on learning (i.e., hippocampal inactivation enhanced latent inhibition of CTA); more novel and surprising, however, was the finding that hippocampal inactivation during training sessions strongly enhanced CTA learning itself. These phenomena were not caused by specific aspects of our infusion technique-muscimol infusions into the hippocampus during familiarization sessions did not cause CTAs, muscimol infusions into gustatory cortex caused the expected attenuation of CTA, and hippocampal inactivation caused the expected attenuation of spatial learning. Thus, we suggest that hippocampal memory processes interfere with the specific learning mechanisms underlying CTA, and more generally that multiple memory systems do not operate independently.
Gustatory stimuli are characterized by a specific hedonic value; they are either palatable or aversive. Hedonic value, along with other psychological dimensions of tastes, is coded in the time-course of gustatory cortex (GC) neural responses and appears to emerge via top-down modulation by the basolateral amygdala (BLA). While the importance of BLA in modulating gustatory cortical function has been well established, the nature of its input onto GC neurons is largely unknown. Somewhat conflicting results from extracellular recordings point to either excitatory or inhibitory effects. Here, we directly test the hypothesis that BLA can evoke time-varying – excitatory and inhibitory – synaptic responses in GC using in vivo intracellular recording techniques in urethane anesthetized rats. Electrical stimulation of BLA evoked a post-synaptic potential (PSP) in GC neurons that resulted from a combination of short and long latency components: an initial monosynaptic, glutamatergic potential followed by a multisynaptic, GABAergic hyperpolarization. As predicted by the dynamic nature of amygdala evoked potentials, trains of five BLA stimuli at rates that mimic physiological firing rates (5–40 Hz) evoke a combination of excitation and inhibition in GC cells. The magnitude of the different components varies depending on the frequency of stimulation, with summation of excitatory and inhibitory inputs reaching its maximum at higher frequencies. These experiments provide the first description of BLA synaptic inputs to GC and reveal that amygdalar afferents can modulate gustatory cortical network activity and its processing of sensory information via time-varying synaptic dynamics.
Neurons in the gustatory cortex (GC) process multiple aspects of a tasting experience, encoding not only the physiochemical identity of tastes, but also their anticipation and hedonic value. Information pertaining to these stimulus features is relayed to GC via the gustatory thalamus (VPMpc) and basolateral amygdala (BLA). It is not known whether these inputs drive separate groups of neurons, thus activating separate channels of information, or are integrated by neurons that receive both afferents. Here, we used anterograde labeling and in vivo intracellular recordings in anesthetized rats to assess the potential convergence of BLA and VPMpc inputs in GC, and to investigate the dynamics of integration of these inputs. We report substantial anatomic overlap of BLA and VPMpc axonal fields across GC, and identify a population of GC neurons receiving converging BLA and VPMpc inputs. Our data show that BLA modulates the gain of VPMpc-evoked responses in a timedependent fashion and that this modulation is dependent on the recruitment of synaptic inhibition by both BLA and VPMpc. Our results suggest that BLA shapes cortical processing of thalamic inputs by dynamically gating the excitatory/inhibitory balance of the GC circuit.
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