The sparseness of the encoding of stimuli by single neurons and by populations of neurons is fundamental to understanding the efficiency and capacity of representations in the brain, and was addressed as follows. The selectivity and sparseness of firing to visual stimuli of single neurons in the primate inferior temporal visual cortex were measured to a set of 20 visual stimuli including objects and faces in macaques performing a visual fixation task. Neurons were analysed with significantly different responses to the stimuli. The firing rate distribution of 36% of the neurons was exponential. Twenty-nine percent of the neurons had too few low rates to be fitted by an exponential distribution, and were fitted by a gamma distribution. Interestingly, the raw firing rate distribution taken across all neurons fitted an exponential distribution very closely. The sparseness a (s) or selectivity of the representation of the set of 20 stimuli provided by each of these neurons (which takes a maximal value of 1.0) had an average across all neurons of 0.77, indicating a rather distributed representation. The sparseness of the representation of a given stimulus by the whole population of neurons, the population sparseness a (p), also had an average value of 0.77. The similarity of the average single neuron selectivity a (s) and population sparseness for any one stimulus taken at any one time a (p) shows that the representation is weakly ergodic. For this to occur, the different neurons must have uncorrelated tuning profiles to the set of stimuli.
Inferior temporal cortex (IT) neurons have reduced receptive field sizes in complex natural scenes. This facilitates the read-out of information about individual objects from IT, but raises the question of whether more than the single object present at the fovea is represented by the firing of IT neurons, as would be important for whole scene perception in which several objects may be located without eye movements. Recordings from IT neurons with five simultaneously presented objects, each subtending 7 degrees , with one object at the fovea and the other four centred 10 degrees eccentrically in the parafovea, showed that although 38 IT neurons had their best response to an effective stimulus at the fovea, eight IT neurons had their best response to an object when it was located in one or more of the parafoveal positions. Moreover, of 54 neurons tested for asymmetric parafoveal receptive fields, 35 (65%) had significantly different responses for different parafoveal positions. The asymmetry was partly related to competition within the receptive fields, as only 21% of the neurons had significant asymmetries when tested with just one object present located at the same parafoveal positions. The findings thus show that some evidence is conveyed by a population of IT neurons about the relative positions of several simultaneously presented objects in a scene extending well into the parafovea during a single fixation, and this is likely to be important in whole scene perception with multiple objects, including specifying the relative positions of different objects in a scene.
. The firing of inferior temporal cortex neurons is tuned to objects and faces, and in a complex scene, their receptive fields are reduced to become similar to the size of an object being fixated. These two properties may underlie how objects in scenes are encoded. An alternative hypothesis suggests that visual perception requires the binding of features of the visual target through spike synchrony in a neuronal assembly. To examine possible contributions of firing synchrony of inferior temporal neurons, we made simultaneous recordings of the activity of several neurons while macaques performed a visual discrimination task. The stimuli were presented in either plain or complex backgrounds. The encoding of information of neurons was analyzed using a decoding algorithm. Ninety-four percent to 99% of the total information was available in the firing rate spike counts, and the contribution of spike timing calculated as stimulus-dependent synchronization (SDS) added only 1-6% of information to the total that was independent of the spike counts in the complex background. Similar results were obtained in the plain background. The quantitatively small contribution of spike timing to the overall information available in spike patterns suggests that information encoding about which stimulus was shown by inferior temporal neurons is achieved mainly by rate coding. Furthermore, it was shown that there was little redundancy (6%) between the information provided by the spike counts of the simultaneously recorded neurons, making spike counts an efficient population code with a high encoding capacity.
A new decoding method is described that enables the information that is encoded by simultaneously recorded neurons to be measured. The algorithm measures the information that is contained not only in the number of spikes from each neuron, but also in the cross-correlations between the neuronal firing including stimulus-dependent synchronization effects. The approach enables the effects of interactions between the 'signal' and 'noise' correlations to be identified and measured, as well as those from stimulus-dependent cross-correlations. The approach provides an estimate of the statistical significance of the stimulus-dependent synchronization information, as well as enabling its magnitude to be compared with the magnitude of the spike-count related information, and also whether these two contributions are additive or redundant. The algorithm operates even with limited numbers of trials. The algorithm is validated by simulation. It was then used to analyze neuronal data from the primate inferior temporal visual cortex. The main conclusions from experiments with two to four simultaneously recorded neurons were that almost all of the information was available in the spike counts of the neurons; that this Rate information included on average very little redundancy arising from stimulus-independent correlation effects; and that stimulus-dependent cross-correlation effects (i.e. stimulus-dependent synchronization) contribute very little to the encoding of information in the inferior temporal visual cortex about which object or face has been presented.
The encoding of information by populations of neurons in the macaque inferior temporal cortex was analyzed using quantitative information-theoretic approaches. It was shown that almost all the information about which of 20 stimuli had been shown in a visual fixation task was present in the number of spikes emitted by each neuron, with stimulus-dependent cross-correlation effects adding for most sets of simultaneously recorded neurons almost no additional information. It was also found that the redundancy between the simultaneously recorded neurons was low, approximately 4% to 10%. Consistent with this, a decoding procedure applied to a population of neurons showed that the information increases approximately linearly with the number of cells in the population.
Perceptual inference refers to the ability to infer sensory stimuli from predictions that result from internal neural representations built through prior experience. Methods of Bayesian statistical inference and decision theory model cognition adequately by using error sensing either in guiding action or in "generative" models that predict the sensory information. In this framework, perception can be seen as a process qualitatively distinct from sensation, a process of information evaluation using previously acquired and stored representations (memories) that is guided by sensory feedback. The stored representations can be utilised as internal models of sensory stimuli enabling long term associations, for example in operant conditioning. Evidence for perceptual inference is contributed by such phenomena as the cortical co-localisation of object perception with object memory, the response invariance in the responses of some neurons to variations in the stimulus, as well as from situations in which perception can be dissociated from sensation. In the context of perceptual inference, sensory areas of the cerebral cortex that have been facilitated by a priming signal may be regarded as comparators in a closed feedback loop, similar to the better known motor reflexes in the sensorimotor system. The adult cerebral cortex can be regarded as similar to a servomechanism, in using sensory feedback to correct internal models, producing predictions of the outside world on the basis of past experience.
Information theoretic analyses showed that for single inferior temporal neurons and neuronal populations, more information was encoded in 20 or more ms by all the spikes available than just by the first spike in the same time window about which of 20 objects or faces was shown. Further, the temporal order in which the first spike arrived from different simultaneously recorded neurons did not encode more information than was present in the first spike or the spike counts. Thus information transmission in the inferior temporal cortex by the number of spikes in even short time windows is fast, and provides more information than only the first spike, or the spike order from different neurons.
Synapse formation and maturation were examined in the rat dorsal lateral geniculate nucleus (dLGN) from birth to adulthood. Examination of animals, whose ages were closely spaced in time, showed that the maturation of the synaptic organization of the nucleus takes place chiefly during the first 3 weeks of postnatal life. This period of maturation may be divided into 3 broad stages. During the first stage, which spans the first 4 days of life, there are only a few immature synapses scattered throughout the nucleus; occasionally aggregates of 3 or 4 synapses are encountered. Dendrodendritic synapses first appear at the end of this stage. The second stage, which lasts from the end of the first stage through day 8, is characterized by intensive synaptogenesis as well as extensive growth and degeneration. For the first time, large boutons resembling retinal terminals form multiple synaptic contacts with dendrites and dendritic protrusions; these synaptic arrangements are partially covered by glial processes. A feature characteristic of the developing dLGN during the first 2 postnatal weeks, and particularly during the second stage, is the presence of membrane specializations that resemble vacant postsynaptic densities. These specializations, which may be unapposed or opposite another neuronal process, decrease in frequency as the number of synapses increases. It is not known whether these densities are converted to synapses or whether they result from loss of presynaptic elements. The third stage in the process of synaptogenesis, which spans a period between days 10 and 20, is characterized by myelination and by the diminution of growth cones, degenerating profiles and vacant postsynaptic densities. There is also a very significant increase in the number and maturation of synapses including synaptic glomeruli. However, it is not until the end of this stage that synapses appear qualitatively indistinguishable from synaptic arrangements identified in adult animals.
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