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Of all of the sensory areas, barrel cortex is among the best understood in terms of circuitry, yet least understood in terms of sensory function. We combined intracellular recording in rats with a multi-directional, multi-whisker stimulator system to estimate receptive fields by reverse correlation of stimuli to synaptic inputs. Spatiotemporal receptive fields were identified orders of magnitude faster than by conventional spike-based approaches, even for neurons with little spiking activity. Given a suitable stimulus representation, a linear model captured the stimulus-response relationship for all neurons with high accuracy. In contrast with conventional single-whisker stimuli, complex stimuli revealed markedly sharpened receptive fields, largely as a result of adaptation. This phenomenon allowed the surround to facilitate rather than to suppress responses to the principal whisker. Optimized stimuli enhanced firing in layers 4-6, but not in layers 2/3, which remained sparsely active. Surround facilitation through adaptation may be required for discriminating complex shapes and textures during natural sensing.

Hebbian models of development and learning require both activity-dependent synaptic plasticity and a mechanism that induces competition between different synapses. One form of experimentally observed long-term synaptic plasticity, which we call spike-timing-dependent plasticity (STDP), depends on the relative timing of pre- and postsynaptic action potentials. In modeling studies, we find that this form of synaptic modification can automatically balance synaptic strengths to make postsynaptic firing irregular but more sensitive to presynaptic spike timing. It has been argued that neurons in vivo operate in such a balanced regime. Synapses modifiable by STDP compete for control of the timing of postsynaptic action potentials. Inputs that fire the postsynaptic neuron with short latency or that act in correlated groups are able to compete most successfully and develop strong synapses, while synapses of longer-latency or less-effective inputs are weakened.

A model for the development of spatiotemporal receptive fields of simple cells in the visual cortex is proposed. The model is based on the 1990 hypothesis of Saul and Humphrey that the convergence of four types of input onto a cortical cell, viz. non-lagged ON and OFF inputs and lagged ON and OFF inputs, underlies the spatial and temporal structure of the receptive fields. It therefore explains both orientation and direction selectivity of simple cells. The response properties of the four types of input are described by the product of linear spatial and temporal response functions. Extending the 1994 model of one of the authors (K.D. Miller), we describe the development of spatiotemporal receptive fields as a Hebbian learning process taking into account not only spatial but also temporal correlations between the different inputs. We derive the correlation functions that drive the development both for the period before and after eye-opening and demonstrate how the joint development of orientation and direction selectivity can be understood in the framework of correlation-based learning. Our investigation is split into two parts that are presented in two papers. In the first, the model for the response properties and for the development of direction-selective receptive fields is presented. In the second paper we present simulation results that are compared with experimental data, and also provide a first analysis of our model.

In part I of this article a correlation based model for the developmental process of spatiotemporal receptive fields has been introduced. In this model the development is described as an activity-dependent competition between four types of input from the lateral geniculate nucleus onto a cortical cell, viz. non-lagged ON and OFF and lagged ON and OFF inputs. In the present paper simulation results and a first analysis are presented for this model. We study the developmental process both before and after eye-opening and compare the results with experimental data from reverse correlation measurements. The outcome of the developmental process is determined mainly by the spatial and the temporal correlations between the different inputs. In particular, if the mean correlation between non-lagged and lagged inputs is weak, receptive fields with a widely varying degree of direction selectivity emerge. However, spatiotemporal receptive fields may show rotation of their preferred orientation as a function of response delay. Even if the mean correlation between two types of temporal input is not weak, direction-selective receptive fields may emerge because of an intracortical interaction between different cortical maps. In an environment of moving lines or gratings, direction-selective receptive fields develop only if the distribution of the directions of motion presented during development shows some anisotropy. In this case, a continuous map of preferred direction is also shown to develop.