Rapid Analysis of Visual Receptive Fields by Iterative Tomography.

Many receptive fields in the early visual system show standard (center-surround) structure and can be analyzed using simple drifting patterns and a difference-of-Gaussians (DoG) model, which treats the receptive field as a linear filter of the visual image. But many other receptive fields show nonlinear properties such as selectivity for direction of movement. Such receptive fields are typically studied using discrete stimuli (moving or flashed bars and edges) and are modelled according to the features of the visual image to which they are most sensitive. Here, we harness recent advances in tomographic image analysis to characterize rapidly and simultaneously both the linear and nonlinear components of visual receptive fields. Spiking and intracellular voltage potential responses to briefly flashed bars are analyzed using non-negative matrix factorization (NNMF) and iterative reconstruction tomography (IRT). The method yields high-resolution receptive field maps of individual neurons and neuron ensembles in primate (marmoset, both sexes) lateral geniculate and rodent (mouse, male) retina. We show that the first two IRT components correspond to DoG-equivalent center and surround of standard [magnocellular (M) and parvocellular (P)] receptive fields in primate geniculate. The first two IRT components also reveal the spatiotemporal receptive field structure of nonstandard (on/off-rectifying) receptive fields. In rodent retina we combine NNMF-IRT with patch-clamp recording and dye injection to directly map spatial receptive fields to the underlying anatomy of retinal output neurons. We conclude that NNMF-IRT provides a rapid and flexible framework for study of receptive fields in the early visual system.

Fractal spike dynamics and neuronal coupling in the primate visual system.

KEY POINTS: We measured fractal (self-similar) fluctuations in ongoing spiking activity in subcortical (lateral geniculate nucleus, LGN) and cortical (area MT) visual areas in anaesthetised marmosets. Cells in the evolutionary ancient koniocellular LGN pathway and in area MT show high-amplitude fractal fluctuations, whereas evolutionarily newer parvocellular and magnocellular LGN cells do not. Spiking activity in koniocellular cells and MT cells shows substantial correlation to the local population activity, whereas activity in parvocellular and magnocellular cells is less correlated with local activity. We develop a model consisting of a fractal process and a global rate modulation which can reproduce and explain the fundamental relationship between fractal fluctuations and population coupling in LGN and MT. The model provides a unified account of apparently disparate aspects of neural spiking activity and can improve our understanding of information processing in evolutionary ancient and modern visual pathways. ABSTRACT: The brain represents and processes information through patterns of spiking activity, which is influenced by local and widescale brain circuits as well as intrinsic neural dynamics. Whether these influences have independent or linked effects on spiking activity is, however, not known. Here we measured spiking activity in two visual centres, the lateral geniculate nucleus (LGN) and cortical area MT, in marmoset monkeys. By combining the Fano-factor time curve, power spectral analysis and rescaled range analysis, we reveal inherent fractal fluctuations of spiking activity in LGN and MT. We found that the evolutionary ancient koniocellular (K) pathway in LGN and area MT exhibits strong fractal fluctuations at short (<1 s) time scales. Parvocellular (P) and magnocellular (M) LGN cells show weaker fractal fluctuations at longer (multi-second) time scales. In both LGN and MT, the amplitude and time scale of fractal fluctuations can explain short and long time scale spiking dynamics. We further show differential neuronal coupling of LGN and MT cells to local population spiking activity. The population coupling is intrinsically linked to fractal fluctuations: neurons showing stronger fluctuations are more strongly correlated to the local population activity. To understand this relationship, we modelled spiking activity using a fractal inhomogeneous Poisson process with dynamic rate, which is the product of an intrinsic stochastic fractal rate and a global modulatory gain. Our model explains the intrinsic links between neuronal spike rate and population coupling in LGN and MT, and establishes a unified account of dynamic spiking properties in afferent visual pathways.

Binocular summation in marmoset lateral geniculate nucleus.

In primates and carnivores, the main laminae of the dorsal lateral geniculate nucleus (LGN) receive monocular excitatory input in an eye-alternating fashion. There is also evidence that nondominant eye stimulation can reduce responses to dominant eye stimulation and that a subset of LGN cells in the koniocellular (K) layers receives convergent binocular excitatory input from both eyes. What is not known is how the two eye inputs summate in the K layers of LGN. Here, we aimed to answer this question by making extracellular array electrode recordings targeted to K layers in the marmoset (Callithrix jacchus) LGN, as visual stimuli (flashed 200 ms temporal square-wave pulses or drifting gratings) were presented to each eye independently or to both eyes simultaneously. We found that when the flashed stimulus was presented to both eyes, compared to the dominant eye, the peak firing rate of most cells (61%, 14/23) was reduced. The remainder showed response facilitation (17%) or partial summation (22%). A greater degree of facilitation was seen when the total number of spikes across the stimulus time window (200 ms) rather than peak firing rates was measured. A similar pattern of results was seen for contrast-varying gratings and for small numbers of parvocellular (n = 12) and magnocellular (n = 3) cells recorded. Our findings show that binocular summation in the marmoset LGN is weak and predominantly sublinear in nature.

Relation of koniocellular layers of dorsal lateral geniculate to inferior pulvinar nuclei in common marmosets.

Traditionally, the dorsal lateral geniculate nucleus (LGN) and the inferior pulvinar (IPul) nucleus are considered as anatomically and functionally distinct thalamic nuclei. However, in several primate species it has also been established that the koniocellular (K) layers of LGN and parts of the IPul have a shared pattern of immunoreactivity for the calcium-binding protein calbindin. These calbindin-rich cells constitute a thalamic matrix system which is implicated in thalamocortical synchronisation. Further, the K layers and IPul are both involved in visual processing and have similar connections with retina and superior colliculus. Here, we confirmed the continuity between calbindin-rich cells in LGN K layers and the central lateral division of IPul (IPulCL) in marmoset monkeys. By employing a high-throughput neuronal tracing method, we found that both the K layers and IPulCL form comparable patterns of connections with striate and extrastriate cortices; these connections are largely different to those of the parvocellular and magnocellular laminae of LGN. Retrograde tracer-labelled cells and anterograde tracer-labelled axon terminals merged seamlessly from IPulCL into LGN K layers. These results support continuity between LGN K layers and IPulCL, providing an anatomical basis for functional congruity of this region of the dorsal thalamic matrix and calling into question the traditional segregation between LGN and the inferior pulvinar nucleus.

Projections of three subcortical visual centers to marmoset lateral geniculate nucleus.

The dorsal lateral geniculate nucleus receives projections from visuotopically organized subcortical nuclei, in addition to inputs from the retina, visual cortices, and the thalamic reticular nucleus. Here, we study subcortical projections to the geniculate from the superior colliculus (SC) and parabigeminal nucleus (PBG) in the midbrain, and the nucleus of the optic tract (NOT) in the pretectum of marmosets. Marmosets are New World diurnal foveate monkeys, and are an increasingly popular model for studying the primate visual system. Furthermore, the koniocellular geniculate layers in marmosets, unlike those in the geniculate of commonly studied diurnal Old World monkeys, are well differentiated from the parvocellular and magnocellular layers. Thus, in the present study, we have made small iontophoretic injections of the retrograde tracer microruby, targeted to the koniocellular layers in the geniculates of four marmosets. We found direct projections from the ipsilateral SC, PBG, and NOT to the koniocellular geniculate layers. The distribution of retrogradely labeled cells in the superficial, visual layers of SC is consistent with the idea that projections from the SC to the koniocellular layers are visuotopically organized. A little over 20 years ago, Vivien Casagrande () introduced the idea that koniocellular geniculate layers (rather than the parvocellular and magnocellular layers) are principal targets of visuotopically organized subcortical nuclei. Our results add to subsequent evidence assembled by Casagrande and others in favor of this hypothesis.

Receptive Field Properties of Koniocellular On/Off Neurons in the Lateral Geniculate Nucleus of Marmoset Monkeys.

The koniocellular (K) layers of the primate dorsal lateral geniculate nucleus house a variety of visual receptive field types, not all of which have been fully characterized. Here we made single-cell recordings targeted to the K layers of diurnal New World monkeys (marmosets). A subset of recorded cells was excited by both increments and decrements of light intensity (on/off-cells). Histological reconstruction of the location of these cells confirmed that they are segregated to K layers; we therefore refer to these cells as K-on/off cells. The K-on/off cells show high contrast sensitivity, strong bandpass spatial frequency tuning, and their response magnitude is strongly reduced by stimuli larger than the excitatory receptive field (silent suppressive surrounds). Stationary counterphase gratings evoke unmodulated spike rate increases or frequency-doubled responses in K-on/off cells; such responses are largely independent of grating spatial phase. The K-on/off cells are not orientation or direction selective. Some (but not all) properties of K-on/off cells are consistent with those of local-edge-detector/impressed-by-contrast cells reported in studies of cat retina and geniculate, and broad-thorny ganglion cells recorded in macaque monkey retina. The receptive field properties of K-on/off cells and their preferential location in the ventral K layers (K1 and K2) make them good candidates for the direct projection from geniculate to extrastriate cortical area MT/V5. If so, they could contribute to visual information processing in the dorsal ("where" or "action") visual stream.SIGNIFICANCE STATEMENT We characterize cells in an evolutionary ancient part of the visual pathway in primates. The cells are located in the lateral geniculate nucleus (the main visual afferent relay nucleus), in regions called koniocellular layers that are known to project to extrastriate visual areas as well as primary visual cortex. The cells show high contrast sensitivity and rapid, transient responses to light onset and offset. Their properties suggest they could contribute to visual processing in the dorsal ("where" or "action") visual stream.

Binocular Visual Responses in the Primate Lateral Geniculate Nucleus.

The dorsal lateral geniculate nucleus (dLGN) in carnivores and primates is a laminated structure, where each layer gets visual input from only one eye [1, 2]. By contrast, in rodents such as mice and rats, the dLGN is not overtly laminated, the retinal terminals from the two eyes are only partially segregated [3, 4], and many cells in the binocular segment of dLGN get excitatory inputs from both eyes [5, 6]. Here, we show that the evolutionary ancient koniocellular (K) division of primate dLGN, like rodent dLGN, forms a subcortical site of binocular integration. We recorded single-cell activity in dLGN of anesthetized marmoset monkeys. As expected, cells in the parvocellular (P) and magnocellular (M) layers received monocular excitatory inputs. By contrast, many cells in the K layers received excitatory inputs from both eyes. The specialized properties of distinct K sub-populations (for example, blue-yellow color selectivity) were preserved across the two eye inputs, and where tested, the contrast sensitivity of each eye input was roughly matched. The results argue that evolutionarily widely separated orders such as rodents and primates have a shared strategy of integrating signals from the two eyes in subcortical circuits.

Binocular neurons in parastriate cortex: interocular 'matching' of receptive field properties, eye dominance and strength of silent suppression.

Spike-responses of single binocular neurons were recorded from a distinct part of primary visual cortex, the parastriate cortex (cytoarchitectonic area 18) of anaesthetized and immobilized domestic cats. Functional identification of neurons was based on the ratios of phase-variant (F1) component to the mean firing rate (F0) of their spike-responses to optimized (orientation, direction, spatial and temporal frequencies and size) sine-wave-luminance-modulated drifting grating patches presented separately via each eye. In over 95% of neurons, the interocular differences in the phase-sensitivities (differences in F1/F0 spike-response ratios) were small (≤ 0.3) and in over 80% of neurons, the interocular differences in preferred orientations were ≤ 10°. The interocular correlations of the direction selectivity indices and optimal spatial frequencies, like those of the phase sensitivies and optimal orientations, were also strong (coefficients of correlation r ≥ 0.7005). By contrast, the interocular correlations of the optimal temporal frequencies, the diameters of summation areas of the excitatory responses and suppression indices were weak (coefficients of correlation r ≤ 0.4585). In cells with high eye dominance indices (HEDI cells), the mean magnitudes of suppressions evoked by stimulation of silent, extra-classical receptive fields via the non-dominant eyes, were significantly greater than those when the stimuli were presented via the dominant eyes. We argue that the well documented 'eye-origin specific' segregation of the lateral geniculate inputs underpinning distinct eye dominance columns in primary visual cortices of mammals with frontally positioned eyes (distinct eye dominance columns), combined with significant interocular differences in the strength of silent suppressive fields, putatively contribute to binocular stereoscopic vision.

Phase sensitivities, excitatory summation fields, and silent suppressive receptive fields of single neurons in the parastriate cortex of the cat.

We have recorded single-neuron activity from cytoarchitectonic area 18 of anesthetized (0.4-0.7% isoflurane in 65% N2O-35% O2 gaseous mixture) domestic cats. Neurons were identified as simple or complex on the basis of the ratios between the phase-variant (F1) component and the mean firing rate (F0) of spike responses to optimized (orientation, direction, spatial and temporal frequencies, size) high-contrast, luminance-modulated, sine-wave drifting gratings (simple: F1/F0 spike-response ratios > 1; complex: F1/F0 spike-response ratios < 1). The predominance (~80%) of simple cells among the neurons recorded from the principal thalamorecipient layers supports the idea that most simple cells in area 18 might constitute a putative early stage in the visual information processing. Apart from the "spike-generating" regions (the classical receptive fields, CRFs), the receptive fields of three-quarters of area 18 neurons contain silent, extraclassical suppressive regions (ECRFs). The spatial extent of summation areas of excitatory responses was negatively correlated with the strength of the ECRF-induced suppression of spike responses. Lowering the stimulus contrast resulted in an expansion of the summation areas of excitatory responses accompanied by a reduction in the strength of the ECRF-induced suppression. The spatial and temporal frequency and orientation tunings of the ECRFs were much broader than those of the CRFs. Hence, the ECRFs of area 18 neurons appear to be largely "inherited" from their dorsal thalamic inputs. In most area 18 cells, costimulation of CRFs and ECRFs resulted in significant increases in F1/F0 spike-response ratios, and thus there was a contextually modulated functional continuum between the simple and complex cells.