A synaptic memory trace for cortical receptive field plasticity

158

Simultaneous presentation of multiple stimuli can reduce the firing rates of neurons in extrastriate visual cortex below the rate elicited by a single preferred stimulus. We describe computational results suggesting how this remarkable effect may arise from strong excitatory drive to a substantial local population of fast-spiking inhibitory interneurons, which can lead to a loss of coherence in that population and thereby raise the effectiveness of inhibition. We propose that in attentional states fast-spiking interneurons may be subject to a bath of inhibition resulting from cholinergic activation of a second class of inhibitory interneurons, restoring conditions needed for gamma rhythmicity. Oscillations and coherence are emergent features, not assumptions, in our model. The gamma oscillations in turn support stimulus competition. The mechanism is a form of ''oscillatory selection,'' in which neural interactions change phase relationships that regulate firing rates, and attention shapes those neural interactions.cholinergic modulation ͉ selective attention ͉ gamma rhythm C ortical gamma frequency (30-90 Hz) oscillations are known to be associated with many aspects of cognition, including sensory processing, attention, memory, and awareness (1). However, the biophysical underpinnings of gamma oscillations and the means by which they contribute to cognitive processing are still not fully understood. Here we continue a series of computational studies investigating how the biophysics of the gamma rhythm, and in particular its neuromodulation, affect network processing associated with attention (2-4).We focus on the much-cited experiments of Desimone and colleagues (5-7). These showed that orientation-selective principal neurons in macaque V2 and V4 respond to simultaneous presentation of preferred (''good'') and nonpreferred (''poor'') stimuli in their receptive fields at spike rates well below those elicited by the preferred stimulus alone. Furthermore, when attention is directed to either of the two stimuli, the neuron responds almost as if the unattended stimulus were absent.The essence of the mechanism we propose here is a relationship between the effectiveness of the excitatory inputs to the target network and the coherence of the network's inhibitory cells: The same drive that produces a robust response when the inhibition is coherent produces a much less robust response when the inhibition is incoherent. We describe how this mechanism can, qualitatively at least, explain the results in (5-7).Selective attention is associated with an increase in coherence of spiking and in spectral power of oscillations in the gamma frequency band (8-10). The model we offer here does not assume a priori that bottom-up or top-down input is made more coherent or more oscillatory as a result of attention (11,12). Rather, the increased gamma power and coherence of the network output are consequences of the biophysical effects of cholinergic modulation. A critical feature of the model is that the target entity of competing stream...

Section: Discussionsupporting

confidence: 88%

Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model

Börgers

Epstein

Kopell

2008

158

“…However, in a recent study of plasticity mediated by nucleus basalis stimulation in the adult auditory cortex, excitation and inhibition underwent a similar transient mismatch of response properties, although the mismatch lasted hours instead of days (34). The similarity of our results in developing visual cortex to those in adult auditory cortex suggests that the transient imbalance of local excitatory and inhibitory cells during change may be a general property of cortical circuit reorganization.…”

Section: Discussionsupporting

confidence: 72%

“…Control (unmanipulated) animals were imaged at ages that spanned the critical period (postnatal days [25][26][27][28][29][30][31][32][33][34][35]. Imaging sessions began with intrinsic signal mapping of the binocular zone to locate the binocular portion of the primary visual cortex.…”

Section: Methodsmentioning

confidence: 99%

Delayed plasticity of inhibitory neurons in developing visual cortex

Gandhi

Yanagawa

Stryker

2008

105

During postnatal development, altered sensory experience triggers the rapid reorganization of neuronal responses and connections in sensory neocortex. This experience-dependent plasticity is disrupted by reductions of intracortical inhibition. Little is known about how the responses of inhibitory cells themselves change during plasticity. We investigated the time course of inhibitory cell plasticity in mouse primary visual cortex by using functional two-photon microscopy with single-cell resolution and genetic identification of cell type. Initially, local inhibitory and excitatory cells had similar binocular visual response properties, both favoring the contralateral eye. After 2 days of monocular visual deprivation, excitatory cell responses shifted to favor the open eye, whereas inhibitory cells continued to respond more strongly to the deprived eye. By 4 days of deprivation, inhibitory cell responses shifted to match the faster changes in their excitatory counterparts. These findings reveal a dramatic delay in inhibitory cell plasticity. A minimal linear model reveals that the delay in inhibitory cell plasticity potently accelerates Hebbian plasticity in neighboring excitatory neurons. These findings offer a network-level explanation as to how inhibition regulates the experiencedependent plasticity of neocortex.inhibition ͉ ocular dominance ͉ two-photon microscopy ͉ calcium imaging ͉ cortical plasticity

“…This parallel instructive signaling at the level of neural circuits and intracellular signaling pathways could enhance the flexibility and computational power of the learning system. This type of teaching signal mechanism may confer an evolutionarily adaptive benefit on the organism and be conserved across neural circuits and species (3,11,16,70). It will be important to determine how these signals are computed in these parallel neural pathways to the LA and how they interact in LA neuronal intracellular signaling networks.…”

Section: Discussionmentioning

confidence: 99%

Hebbian and neuromodulatory mechanisms interact to trigger associative memory formation

Johansen

Díaz-Mataix

Hamanaka

et al. 2014

168

138

A long-standing hypothesis termed "Hebbian plasticity" suggests that memories are formed through strengthening of synaptic connections between neurons with correlated activity. In contrast, other theories propose that coactivation of Hebbian and neuromodulatory processes produce the synaptic strengthening that underlies memory formation. Using optogenetics we directly tested whether Hebbian plasticity alone is both necessary and sufficient to produce physiological changes mediating actual memory formation in behaving animals. Our previous work with this method suggested that Hebbian mechanisms are sufficient to produce aversive associative learning under artificial conditions involving strong, iterative training. Here we systematically tested whether Hebbian mechanisms are necessary and sufficient to produce associative learning under more moderate training conditions that are similar to those that occur in daily life. We measured neural plasticity in the lateral amygdala, a brain region important for associative memory storage about danger. Our findings provide evidence that Hebbian mechanisms are necessary to produce neural plasticity in the lateral amygdala and behavioral memory formation. However, under these conditions Hebbian mechanisms alone were not sufficient to produce these physiological and behavioral effects unless neuromodulatory systems were coactivated. These results provide insight into how aversive experiences trigger memories and suggest that combined Hebbian and neuromodulatory processes interact to engage associative aversive learning.Hebbian plasticity | amygdala | neuromodulation | instructive signals | associative learning H ebbian plasticity refers to the strengthening of a presynaptic input onto a postsynaptic neuron when both pre-and postsynaptic neurons are coactive (1). This was originally proposed as a mechanism for memory formation. Findings from in vitro and in vivo physiological studies suggest that Hebbian processes control synaptic strengthening (2-10). However, other results and theories suggest that Hebbian mechanisms alone are not normally sufficient for producing synaptic plasticity and that synaptic strengthening mediating memory formation involves interactions between Hebbian and neuromodulatory mechanisms (3,4,7,(11)(12)(13)(14)(15)(16)(17)(18)(19). Although molecules that may mediate Hebbian processes in memory formation have been identified (3,11,16,17,(20)(21)(22), it has been difficult to directly test whether Hebbian plasticity alone or in combination with neuromodulation is necessary and sufficient to produce neural plasticity and memories in behaving animals (especially in mammals). This is because of technical limitations in controlling correlated activity between pre-and postsynaptic neurons involved in memory storage in a temporally/spatially precise manner while measuring behavioral memory formation and neural plasticity.To overcome these problems, we used optogenetic techniques to directly manipulate Hebbian mechanisms in pyramidal neurons in the lateral nucl...