Sensory experience modifies spontaneous state dynamics in a large-scale barrel cortical model

Experimental evidence suggests that spontaneous neuronal activity may shape and be shaped by sensory experience. However, we lack information on how sensory experience modulates the underlying synaptic dynamics and how such modulation influences the response of the network to future events. Here we study whether spike-timing-dependent plasticity (STDP) can mediate sensory-induced modifications in the spontaneous dynamics of a new large-scale model of layers II, III and IV of the rodent barrel cortex. Our model incorporates significant physiological detail, including the types of neurons present, the probabilities and delays of connections, and the STDP profiles at each excitatory synapse. We stimulated the neuronal network with a protocol of repeated sensory inputs resembling those generated by the protraction-retraction motion of whiskers when rodents explore their environment, and studied the changes in network dynamics. By applying dimensionality reduction techniques to the synaptic weight space, we show that the initial spontaneous state is modified by each repetition of the stimulus and that this reverberation of the sensory experience induces long-term, structured modifications in the synaptic weight space. The post-stimulus spontaneous state encodes a memory of the stimulus presented, since a different dynamical response is observed when the network is presented with shuffled stimuli. These results suggest that repeated exposure to the same sensory experience could induce long-term circuitry modifications via 'Hebbian' STDP plasticity.     

Pontogeniculooccipital waves: spontaneous visual system activity during rapid eye movement sleep

1. Pontogeniculooccipital (PGO) waves are recorded during rapid eye movement (REM) sleep from the pontine reticular formation, lateral geniculate bodies, and occipital cortex of many species. 2. PGO waves are associated with increased visual system excitability but arise spontaneously and not via stimulation of the primary visual afferents. Both auditory and somatosensory stimuli influence PGO wave activity. 3. Studies using a variety of techniques suggest that the pontine brain stem is the site of PGO wave generation. Immediately prior to the appearance of PGO waves, neurons located in the region of the brachium conjunctivum exhibit bursts of increased firing, while neurons in the dorsal raphe nuclei show a cessation of firing. 4. The administration of pharmacological agents antagonizing noradrenergic or serotonergic neurotransmission increases the occurrence of PGO waves independent of REM sleep. Cholinomimetic administration increases the occurrence of both PGO waves and other components of REM sleep. 5. Regarding function, the PGO wave-generating network has been postulated to inform the visual system about eye movements, to promote brain development, and to facilitate the response to novel environmental stimuli.     

A desert ant's memory of recent visual experience and the control of route guidance

Insects such as desert ants learn stereotyped visual routes between their nests and reliable food sites. Studies here reveal an important control element for ensuring that the route memories are used appropriately. They find that visual route memories can be disengaged, so that they do not provide guidance, even when all appropriate visual cues are present and when there are no competing guidance cues. Ants were trained along a simple route dominated by a single isolated landmark. If returning ants were caught just before entering the nest and replaced at the feeder, then they often interrupted the recapitulation of their homeward route with a period of apparent confusion during which the route memories were ignored. A series of experiments showed that this confusion occurred in response to the repetition of the route, and that the ants must therefore maintain some kind of a memory of their visual experience on the current trip home. A conceptual model of route guidance is offered to explain the results here. It proposes how the memory might act and suggests a general role for disengagement in regulating route guidance.     

Direction selectivity in the retina is established independent of visual experience and cholinergic retinal waves

Direction selectivity in the retina requires the asymmetric wiring of inhibitory inputs onto four subtypes of On-Off direction-selective ganglion cells (DSGCs), each preferring motion in one of four cardinal directions. The primary model for the development of direction selectivity is that patterned activity plays an instructive role. Here, we use a unique, large-scale multielectrode array to demonstrate that DSGCs are present at eye opening, in mice that have been reared in darkness and in mice that lack cholinergic retinal waves. These data suggest that direction selectivity in the retina is established largely independent of patterned activity and is therefore likely to emerge as a result of complex molecular interactions.     

Postnatal development of functional properties of the visual cortical cells of area 18 in kittens raised with or without visual experience

866 units were recorded extracellularly in area 18 of anaesthetized and paralysed kittens from 13 to 66 days of age. The development of their receptive field properties was studied in normally (EN) and dark-reared (EO) kittens. In addition to orientation selective (S) and non-selective (NS) cells, we found a number of non-selective units whose receptive field was surrounded by a peripheral zone (NSp) where stationary stimuli were effective. In EN kittens, the orientation selectivity developed with age and concomitantly, NS and NSp cells disappeared. Ocular dominance distribution was also gradually modified from a contralateral monocular dominance at 13 days of age to an adult-like binocularity at 58 days. In EO kittens, the early orientation selectivity began to decrease at the 5th week. From then on, the process of despecification started and progressed until nearly all cells were NS. Absence of visual experience also delayed the development of mature binocularity. In 6 week old EO kittens, a 6 hrs. visual exposure induced a fast but uncomplete specification with decrease of both NS and NSp cells and a slight modification of the ocular dominance distribution. The comparison of these results with those obtained in area 17 shows that functional properties vary more slowly in area 18 than in area 17.     

Mechanobiology in cortical waves and oscillations

Cortical actin waves have emerged as a widely prevalent phenomena and brought pattern formation to many fields of cell biology. Cortical excitabilities, reminiscent of the electric excitability in neurons, are likely fundamental property of the cell cortex. Although they have been mostly considered to be biochemical in nature, accumulating evidence support the role of mechanics in the pattern formation process. Both pattern formation and mechanobiology approach biological phenomena at the collective level, either by looking at the mesoscale dynamical behavior of molecular networks or by using collective physical properties to characterize biological systems. As such they are very different from the traditional reductionist, bottom-up view of biology, which brings new challenges and potential opportunities. In this essay, we aim to provide our perspectives on what the proposed mechanochemical feedbacks are and open questions regarding their role in cortical excitable and oscillatory dynamics.     

Traveling waves in visual cortex

Electrode recordings and imaging studies have revealed that localized visual stimuli elicit waves of activity that travel across primary visual cortex. Traveling waves are present also during spontaneous activity, but they can be greatly reduced by widespread and intensive visual stimulation. In this Review, we summarize the evidence in favor of these traveling waves. We suggest that their substrate may lie in long-range horizontal connections and that their functional role may involve the integration of information over large regions of space.     

Adult visual cortical plasticity

The visual cortex has the capacity for experience-dependent change, or cortical plasticity, that is retained throughout life. Plasticity is invoked for encoding information during perceptual learning, by internally representing the regularities of the visual environment, which is useful for facilitating intermediate-level vision-contour integration and surface segmentation. The same mechanisms have adaptive value for functional recovery after CNS damage, such as that associated with stroke or neurodegenerative disease. A common feature to plasticity in primary visual cortex (V1) is an association field that links contour elements across the visual field. The circuitry underlying the association field includes a plexus of long-range horizontal connections formed by cortical pyramidal cells. These connections undergo rapid and exuberant sprouting and pruning in response to removal of sensory input, which can account for the topographic reorganization following retinal lesions. Similar alterations in cortical circuitry may be involved in perceptual learning, and the changes observed in V1 may be representative of how learned information is encoded throughout the cerebral cortex.     

Bimodal septal and cortical triggering and complex propagation patterns of spontaneous waves of activity in the developing mouse cerebral cortex

Spontaneous waves of activity that propagate across large structures during specific developmental stages play central roles in CNS development. To understand the genesis and functions of these waves, it is critical to understand the spatial and temporal patterns of their propagation. We recently reported that spontaneous waves in the neonatal cerebral cortex originate from a ventrolateral pacemaker region. We have now analyzed a large number of spontaneous waves using calcium imaging over the entire area of coronal slices from E18‐P1 mouse brains. In all waves, the first cortical region active is this ventrolateral pacemaker. In half of the waves, however, the cortical pacemaker activity is itself triggered by preceding activity in the septal nuclei. Most waves are restricted to the septum and/or ventral cortex, with only some invading the dorsal cortex or the contralateral hemisphere. Waves fail to propagate at very stereotyped locations at the boundary between ventral and dorsal cortex and at the dorsal midline. Waves that cross these boundaries pause at these same locations. Waves at these stages are blocked by both picrotoxin and CNQX, indicating that both GABA_A and AMPA receptors are involved in spontaneous activity. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70: 679–692, 2010     

Instructive effect of visual experience in mouse visual cortex

We describe a form of experience-dependent response enhancement in the visual cortex of awake mice. Repeated presentations of grating stimuli of a single orientation result in a persistent enhancement of responses evoked by the test stimulus. Response potentiation is specific to the orientation of the test stimulus, develops gradually over the course of several training sessions, and occurs in both juvenile and adult mice. The stimulus-selective response potentiation (SRP) can mask deprivation-induced response depression in adult mice. SRP requires NMDA receptor activation and is prevented by viral delivery of a peptide that interferes with AMPA receptor trafficking. SRP may reveal the mechanisms involved in certain forms of perceptual learning.     

Laminar processing in the visual cortical column

Sensory regions of neocortex are organized as arrays of vertical columns composed of cells that share similar response properties, with the orientation columns of the cat's visual cortex being the best known example. Interest in how sensitivity to different stimulus features first emerges in the columns and how this selectivity is refined by subsequent processing has fueled decades of research. A natural starting point in approaching these issues is anatomy. Each column traverses the six cortical layers and each layer has a unique pattern of inputs, intrinsic connections and outputs. Thus, it makes sense to explore the possibility of corresponding laminar differences in sensory function, that is, to examine relationships between morphology and physiology. In addition, to help identify general patterns of cortical organization, it is useful to compare results obtained from different sensory systems and diverse species. The picture that emerges from such comparisons is that each cortical layer serves a distinct role in sensory function. Furthermore, different cortices appear to share some common strategies for processing information but also have specialized mechanisms adapted for the demands of specific sensory tasks.     

Temporal summation in cat visual cortical neurons

Characteristics of temporal summation in neurons of area 17 of the visual cortex in acute experiments on unanesthetized, immobilized cats. During light adaptation, extracellular spike responses of these neurons to optimal local photic stimuli of varied duration — from 5 to 1000 msec — were studied. The critical duration of temporal summation of excitation, determined by the supraliminal method using the criterion of maximal discharge frequency in the first volley of the spike response, varied in different cells from 5 to 100 msec; neurons with summation lasting 15–100 msec (mean 31.45±5.67 msec) were found most frequently. Neurons with central receptive fields differed significantly from cellswith peripheral fields in the shorter critical duration of temporal summation, the lower frequency of spontaneous discharges, and the shorter duration of the first volley of the response. Summation time in neurons with simple receptive fields was significantly shorter than in neurons with complex receptive fields. The results of these experiments are compared with data in the literature obtained by the study of retinal and lateral geniculate neurons in cats and are discussed from the stand-point of division of ascending afferent projections in the visual system into X-and Y-groups (Ia and Ib).Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 13, No. 4, pp. 345–352, July–August, 1981.     

Standing waves and traveling waves distinguish two circuits in visual cortex

The visual cortex represents stimuli through the activity of neuronal populations. We measured the evolution of this activity in space and time by imaging voltage-sensitive dyes in cat area V1. Contrast-reversing stimuli elicit responses that oscillate at twice the stimulus frequency, indicating that signals originate mostly in complex cells. These responses stand clear of the noise, whose amplitude decreases as 1/frequency, and yield high-resolution maps of orientation preference and retinotopy. We first show how these maps are combined to yield the responses to focal, oriented stimuli. We then study the evolution of the oscillating activity in space and time. In the orientation domain, it is a standing wave. In the spatial domain, it is a traveling wave propagating at 0.2-0.5 m/s. These different dynamics indicate a fundamental distinction in the circuits underlying selectivity for position and orientation, two key stimulus attributes.     

视觉编码的快速学习

活动依赖的神经可塑性在视觉皮层信息处理过程中起着很重要的作用。该文将讲述几个关于视觉刺激引起皮层反应发生快速变化的研究工作。在体膜片钳的实验结果表明,将视觉刺激与能够诱发孽个视皮层神经元发放动作电位的电刺激相偶联可以改变神经元的感受野特性。单电极和多电极胞外记录的实验结果显示,反复地给予自然图形电影刺激,不仅能增加视皮层神经元反应的可靠性,而且能造成之后的自发活动中存在“记忆的痕迹”。最后,用电压敏感染料成像的方法对群体细胞活动进行考察,结果提示视觉活动之后的皮层回放可能是由皮层波介导的。     

Functional characteristics of visual cortical neurons in squirrels

Depending on the organization of their receptive fields and character of their responses to shaped visual stimuli the following main groups of visual cortical neurons were distinguished in the squirrelSciurus vulgaris: nonselective for direction of movement and orientation of stimuli (14%); selective for direction of movement (30%) and selective for line orientation (49%); 7% of neurons were not classified. Cells selective for direction of movement and some nonselective cells exhibited specific sensitivity to high speeds of stimulus movement (optimal velocities of the order of hundreds of degrees per second). Neurons selective for line orientation differed in the degree of overlapping of their on- and off-zones; they could include analogs of simple and complex neurons.A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Moscow. Translated from Neirofiziologiya, Vol. 13, No. 2, pp. 125–231, March–April, 1981.