Norepinephrine Potentiates and Serotonin Depresses Visual Cortical Responses by Transforming Eligibility Traces

Reinforcement allows organisms to learn which stimuli predict subsequent biological relevance. Hebbian mechanisms of synaptic plasticity are insufficient to account for reinforced learning because neuromodulators signaling biological relevance are delayed with respect to the neural activity associated with the stimulus. A theoretical solution is the concept of eligibility traces (eTraces), silent synaptic processes elicited by activity which upon arrival of a neuromodulator are converted into a lasting change in synaptic strength. Previously we demonstrated in visual cortical slices the Hebbian induction of eTraces and their conversion into LTP and LTD by the retroactive action of norepinephrine and serotonin Here we show in vivo in V1 that the induction of eTraces and their conversion to LTP/D by norepinephrine and serotonin respectively potentiates and depresses visual responses. We also show that the integrity of this process is crucial for ocular dominance plasticity, a canonical model of experience-dependent plasticity.

Indexing sensory plasticity: Evidence for distinct Predictive Coding and Hebbian Learning mechanisms in the cerebral cortex

The Roving Mismatch Negativity (MMN), and Visual LTP paradigms are widely used as independent measures of sensory plasticity. However, the paradigms are built upon fundamentally different (and seemingly opposing) models of perceptual learning; namely, Predictive Coding (MMN) and Hebbian plasticity (LTP). The aims of the current study were to 1) compare the generative mechanisms of the MMN and visual LTP, therefore assessing whether Predictive Coding and Hebbian mechanisms co-occur in the brain, and 2) assess whether the paradigms identify similar group differences in plasticity. Forty participants were split into two groups based on the BDNF Val66Met polymorphism and were presented with both paradigms. Consistent with Predictive Coding and Hebbian predictions, Dynamic Causal Modelling revealed that the generation of the MMN modulates forward and backward connections in the underlying network, while visual LTP only modulates forward connections. Genetic differences were identified in the ERPs for both paradigms, but were only apparent in backward connections of the MMN network. These results suggest that both Predictive Coding and Hebbian mechanisms are utilized by the brain under different task demands. Additionally, both tasks provide unique insight into plasticity mechanisms, which has important implications for future studies of aberrant plasticity in clinical populations.

The dialectic of Hebb and homeostasis

It has become widely accepted that homeostatic and Hebbian plasticity mechanisms work hand in glove to refine neural circuit function. Nonetheless, our understanding of how these fundamentally distinct forms of plasticity compliment (and under some circumstances interfere with) each other remains rudimentary. Here, I describe some of the recent progress of the field, as well as some of the deep puzzles that remain. These include unravelling the spatial and temporal scales of different homeostatic and Hebbian mechanisms, determining which aspects of network function are under homeostatic control, and understanding when and how homeostatic and Hebbian mechanisms must be segregated within neural circuits to prevent interference. This article is part of the themed issue ‘Integrating Hebbian and homeostatic plasticity’.

Plasticity in the acquisition of multisensory integration capabilities in superior colliculus

The multisensory integration capabilities of superior colliculus (SC) neurons are normally acquired during early postnatal life and adapted to the environment in which they will be used. Recent evidence shows that they can even be acquired in adulthood, and require neither consciousness nor any of the reinforcement contingencies generally associated with learning. This process is believed to be based on Hebbian mechanisms, whereby the temporal coupling of multiple sensory inputs initiates development of a means of integrating their information. This predicts that co-activation of those input channels is sufficient to induce multisensory integration capabilities regardless of the specific spatiotemporal properties of the initiating stimuli. However, one might expect that the stimuli to be integrated should be consonant with the functional role of the neurons involved. For the SC, this would involve stimuli that can be localized. Experience with a non-localizable cue in one modality (e.g., ambient sound) and a discrete stimulus in another (e.g., a light flash) should not be sufficient for this purpose. Indeed, experiments with cats reared in omnidirectional sound (effectively masking discrete auditory events) reveal that the simple co-activation of two sensory input channels is not sufficient for this purpose. The data suggest that experience with the kinds of cross-modal events that facilitate the role of the SC in detecting, locating, and orienting to localized external events is a guiding factor in this maturational process. Supported by NIH grants NS 036916 and EY016716.

Segregation of on and offRetinogeniculate Connectivity Directed by Patterned Spontaneous Activity

In many parts of the developing nervous system, the early patterns of connectivity are refined by processes that require neuronal activity. These processes are thought to involve Hebbian mechanisms that lead to strengthening and maintenance of inputs that display correlated pre- and postsynaptic activity and elimination of inputs that fire asynchronously. Here we investigated the role of patterned spontaneous retinal activity and Hebbian synaptic mechanisms on segregation of on and off retinal afferents in the dorsal lateral geniculate nucleus (dLGN) of the developing ferret visual system. We recorded extracellularly the spontaneous spike activity of neighboring pairs of ganglion cells and found thatoff cells have significantly higher mean firing rates thanon cells. Spiking is best correlated between cells of the same sign (on, on; off,off) compared with cells of opposite sign (on,off). We then constructed a simple Hebbian model of retinogeniculate synaptic development based on a correlational framework. Using our recorded activity patterns, together with previous calcium-imaging data, we show that endogenous retinal activity, coupled with Hebbian mechanisms of synaptic development, can drive the segregation of on and off retinal inputs to the dLGN. Segregation occurs robustly when heterosynaptic competition is present within time windows of 50–500 ms. In addition, our results suggest that the initial patterns of connectivity (biases in convergence of inputs) and the strength of inhibition in the network each play a crucial role in determining whether on oroff inputs dominate at maturity.

An evolutionary perspective on Hebb's reverberatory representations

Hebbian mechanisms are justified according to their functional utility in an evolutionary sense. The selective advantage of correlating content-contingent stimuli reflects the putative common cause of temporally or spatially contiguous inputs. The selective consequences of such correlations are discussed by using examples from the evolution of signal form in sexual selection and model-mimic coevolution. We suggest that evolutionary justification might be considered in addition to neurophysiology plansibility when constructing representational models.