Ординатура / Офтальмология / Английские материалы / Progress in Brain Research Visual Perception, Part I Fundamentals of Vision Low and Mid-Level Processes in Perception_2006

with similar-sized CTB injections in the same area of the same species (compare EGFP-labeled corticocortical connections in Stettler et al., 2002, with CTB-labeled corticocortical connections in Angelucci et al. 2002b). We conclude that, at present, CTB is a superior axonal tracing method, and is better suited to labeling long-range corticocortical connections than the adenovirus-EGFP method. The studies by Rockland’ s group (Rockland, 2003), instead, may have failed to observe patterned FB terminations because these authors sectioned V1 in the pia-to-white matter plane. This was motivated by their need to reconstruct individual axons, which can be best followed in this plane of sectioning. Tangential sectioning of flattened and unfolded cortex can reveal patterns that are otherwise difficult to observe in the pia- to-white matter plane (Sincich et al., 2003).

While differences in tracing methods may explain the discrepancy between different studies on the patterning of FB connections, an alternative or additional explanation is that differences in the patterning and specificity of FB connections may reflect placement of tracer injections in different cortical layers or different compartments of extrastriate cortex, or it may reflect the V1 layers of FB termination analyzed in the different studies. Our unpublished data strongly suggests that clustering of FB terminals in area V1 is independent of the extrastriate area, CO compartment and cortical layer of origin of the FB connections. It is also independent of primate species. Specifically, tracer injections (BDA or CTB) in the thick or pale CO stripes of marmoset or macaque area V2 (Fig. 6) and in macaque area V3 (Fig. 7) produce patchy FB terminations in layers 2/3, 4B and 5/6. Following V3 injections, the patches in V1 align either with the CO blobs or interblobs, suggesting placement of tracer injections in different compartments of V3. In layers 2/3 and 4B, the patches of FB terminals are spatially coincident with patches of retrogradely labeled cells sending ascending FF projections (Figs. 6c, f, 7b, h). The FB patches in layer 6, instead, consist predominantly of anterograde label with only occasional retrogradely labeled cell bodies (Figs. 6g, 7c–d). This FB pathway to V1 layers 6 is only labeled when the tracer injections involve layer 6 of extrastriate cortex, but

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not if the injections involve only the upper layers. Thus, there appears to exist a layer-6-to-layer-6 FB pathway that is not reciprocated by a significant FF pathway from V1 layer 6. We conclude that FB connections to V1 layers 2/3, 4B and 6, much like the FF connections from these V1 layers to areas V2 and V3, terminate in a patchy fashion, and that this patterning is independent of the extrastriate area or CO compartment of origin or primate species. Patchy FB connections to V1 layers 2/3, 4B and 5/6 are also observed regardless of whether the tracer injection involves only layers 2/3 (Fig. 7i) or all layers of extrastriate cortex (Fig. 7e).

In agreement with previous reports of diffuse FB connections to V1 layer 1 (Rockland and Pandya, 1979; Ungerleider and Desimone, 1986; Shmuel et al., 2005), our data show that the patterning of FB terminations to V1 is instead dependent on the target layer, as FB connections to layer 1 terminate in a diffuse fashion. The same BDA or CTB injections in V2 of macaque and marmoset monkeys that produced patchy FB connections in the deep V1 layers, labeled sparse and diffuse fibers in layer 1 (Fig. 6b, e). What is novel about our data on FB connections to layer 1, is that we found these connections to form different terminal patterns in the upper and lower halves of this layer. Specifically, while FB connections to V1 layer 1A terminate in a diffuse fashion (Fig. 6b, e), they form terminal clusters in layer 1B (Fig. 6h). As there are no FF projections arising from layer 1 of V1, the clusters of anterograde label in layer 1B occur in the absence of any retrograde label in the same layer. That layer 1 can be subdivided into an upper (1A) and lower (1B) layer was previously proposed on the basis of distinct patterns of anatomical markers and anatomical connections observed in these sub-layers (Ichinohe et al., 2003; Ichinohe and Rockland, 2004). These studies have also demonstrated a modular organization of specific markers in lower layer 1 (Ichinohe et al., 2003). On the basis of these results, it is possible that Stettler et al. (2002) failed to observe patterned FB terminations in V1, because they may have collapsed onto a single plane their anatomical reconstructions of FB label in layers 1–3, thus intermingling clustered and unclustered FB terminations in these different

layers. Indeed, it appears that these authors did not always have interleaved CO-stained sections in V1, and thus their identification of V1 layers may not have always been accurate.

Thus, our results suggest the existence of at least two differently organized systems of FB connections to V1, one patchy and specific, terminating in layers 1B, 2/3, 4B and 5/6, the other diffuse and unspecific, terminating in layer 1A. The clustering and functional specificity of the patchy FB system are consistent with their proposed role in mediating orientation-specific and attribute-specific influences from the far extra-classical surround of V1 neurons. A role for the diffuse FB systems remains to be determined.

The contribution of feedforward, lateral and feedback connections to the receptive field center and surround of V1 neurons: a neural network model and its experimental validation

The data reviewed above on the spatio-temporal properties and functional organization of FF, lateral and FB connections have led us to suggest a specific hypothesis on the relative contribution of these connections to the RF center and surround of V1 neurons. We suggest that geniculate FF connections generate responses within the hsRF

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size of V1 neurons. V1 lateral and extrastriate FB connections enhance such responses. Modulation of RF center responses from the near surround region outside the hsRF is mediated by lateral and FB connections, while far surround modulation is generated by FB connections. This hypothesis, and the main data underlying it, is schematically depicted in Fig. 8a.

Data on the spatio-temporal properties and functional organization of FF, lateral and FB connections were incorporated in a simplified recurrent network model of center–surround interactions, specifically designed to test our hypothesis and to make specific predictions (Schwabe et al., 2006). The basic model architecture, constrained by these data, is depicted in Fig. 8b. The model consists of two interconnected visual areas, one corresponding to V1 and the other to an extrastriate area such as MT. In the absence of feedback, our model essentially reduces to a class of recurrent network models previously used to explore the role of lateral connections in center– surround interactions (Somers et al., 1998; Dragoi and Sur, 2000). These models assume that stimulation of the near surround modulates the response to a center stimulus via lateral connections targeting both excitatory and inhibitory neurons in the center. If the interneurons are taken to have higher threshold and gain than the local excitatory

neurons whose output they control (Lund et al., 1995), then they only generate suppression under sufficiently high levels of excitation, for example, when the contrast and/or size of a grating stimulus in the RF center is sufficiently large. At low levels of excitation, such as for small or low-contrast stimuli, the inhibitors are inactive and stimulation of the near surround facilitates the center response, thus providing an explanation for the expansion of the sRF at low stimulus contrast.

In order to account for the fast onset and large spatial extent of surround suppression, we have extended these models by assuming that (i) FB from extrastriate cortex provides an additional source of excitation to excitatory neurons in the center and near surround; (ii) fast suppression from the far surround occurs via FB, rather than via a cascade of lateral connections. It is noteworthy that our proposed role for FB connections in far surround suppression may appear to be inconsistent with the experimental finding (see above) that FB axons arising from excitatory neurons in extrastriate cortex target almost exclusively (97–98%)

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excitatory neurons in V1 (Johnson and Burkhalter, 1996). Our model, instead, provides an explanation for how exclusively excitatory inter-areal FB, targeting predominantly excitatory neurons, can mediate far surround suppression of the center neurons; namely by targeting excitatory neurons in the near surround, which in turn, via lateral connections, excite the local inhibitory neurons in the center. We have recently shown how our model can account for a wide range of physiological data regarding the static and dynamic effects of surround suppression (Schwabe et al., 2006). These include: (1) the expansion of the sRF at low stimulus contrast (Kapadia et al., 1999; Sceniak et al., 1999); (2) the size-tuning curves of V1 neurons (Sceniak et al., 2001; Cavanaugh et al., 2002; Levitt and Lund, 2002); (3) far surround suppression, as shown in experiments in which the afferent drive to near surround neurons sending lateral connections to the center was partially withdrawn by interposing a blank stimulus between a grating in the RF center and a grating in the far surround (Levitt and Lund, 2002); (4) FB-mediated facilitation of

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responses to stimuli in the RF center, and FBmediated suppression of responses to stimuli in the RF center by stimuli in the surround, as demonstrated by experiments in which FB connections were inactivated (Hupe´et al., 1998; Bullier et al., 2001); (5) the latency and dynamics of surround suppression (Bair et al., 2003).

Our model makes the novel prediction that stimulation of the far surround can suppress or facilitate the RF center response, depending on the total amount of excitatory drive to the local inhibitors. In Fig. 9a we show the results of a model simulation, in which a high contrast annular grating was presented in the far surround together with a central high-contrast grating fitted to the size of the neuron’s hsRF. The inner radius of the annulus was systematically decreased from the far surround to a size no smaller than that of the lsRF, so that the near surround neurons in the lsRF but beyond the hsRF never received afferent stimulation. This minimized the stimulation of neurons

sending monosynaptic lateral connections to the center neuron and allowed us to unmask FBmediated influences from the far surround. As the inner radius of the annulus was decreased, more neurons in the far surround receive afferent stimulation. This led to suppression of the excitatory neurons in the center (solid black curve in Fig. 9a), as previously observed experimentally (Levitt and Lund, 2002). On the other hand, when a lowcontrast central stimulus was presented together with a high-contrast annulus in the far surround, decreasing the inner radius of the annulus could lead to initial facilitation of the center excitatory neurons followed by suppression (solid gray curve in Fig. 9a). This is due to the fact that the lowcontrast central stimulus is too weak to activate the center interneurons by itself; thus, stimulation of the far surround initially facilitates the response of the center neurons, because FB inputs to the center sum with afferent and lateral inputs, until a critical annulus size is reached, beyond which the

interneurons are activated (dashed gray curve in Fig. 9a) and suppression occurs. This prediction is consistent with our recent physiological data (Ichida et al., 2005); two sample cells are shown in Fig. 9b. As in the model, and as previously demonstrated (Levitt and Lund, 2002), presentation of a high-contrast annular grating in the far surround suppressesed the RF center response to a highcontrast central grating (black curves in Fig. 9b). However, as predicted by the model, as the inner radius of a high-or low-contrast annular grating in the surround was reduced, we observed first facilitation and then suppression of the RF center response to a low-contrast central grating (gray curves in Fig. 9b). We have observed facilitation from the far surround in 450% of cells. Furthermore, for any given cell facilitation peaked at smaller inner radii when the stimulus contrast in the surround was also lowered (not shown). Note that cascading lateral connections are unlikely to contribute to the modulatory effects of the far surround in these experiments, because excitatory neurons whose RFs lie in the visual field location of the blank stimulus do not receive afferent drive, and thus cannot effectively relay signals to their postsynaptic V1 neurons. These findings demonstrate that the ‘‘suppressive surround’’ of V1 neurons is not always suppressive, and are thus inconsistent with the DOG model of cen- ter–surround interactions (Fig. 2b). More generally, our model provides a general mechanism of how top–down signals can shape the extraclassical RF of cortical neurons. The same model can also be easily extended to account for the effects of spatial attention in V1.

Conclusions

Studies on the spatio-temporal properties, patterning and functional specificity of FF, lateral and FB connections are beginning to shed some light on the relative roles of each system of connections in the generation of responses within and outside the classical RF of V1 neurons. We have now gathered enough anatomical and physiological data to constrain our neural network models, and to use such models to test specific hypotheses

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on the mechanisms by which these connections can generate V1 neuron responses.

Our data and modeling results so far have led us to think that the RF center and surround of V1 neurons result from integration of signals from all three sets of connections, FF, lateral and FB. These connections operate at different spatial scales, and all send excitatory inputs to neurons in the RF center. Lateral connections, but possibly not FF or FB connections, also contact local inhibitory neurons, which in turn control the output of the center excitatory neurons. FB connections can exert suppression via lateral excitation of local inhibitors. As these inhibitors have higher threshold and gain than the center excitatory neurons, they are only engaged when a significant amount of excitation leads them to fire. Thus, weak stimuli (such as bars, low-contrast or small high-contrast gratings) most often facilitate, whereas strong stimuli (such as high-contrast large gratings) most often suppress the center neurons.

The RF center of V1 neurons is initially generated by driving FF inputs arising from the LGN. Specifically, the mRF, i.e. the spiking region of the RF, is generated by converging inputs from the classical RF center of geniculate cells whose response is at the peak of their size tuning curve. The hsRF of V1 cells, i.e. the subthreshold depolarizing region surrounding the mRF, results from converging inputs from the classical RF center plus surround of geniculate neurons whose response is partially attenuated, due to surround suppression of LGN cells. V1 lateral connections and extrastriate FB connections also contribute to the mRF and hsRF of V1 neurons, by enhancing the neuron response. Stimuli outside the hsRF can influence the center neuron’s response only via lateral and FB connections, and can evoke facilitation or suppression depending on the total amount of excitatory drive reaching the local inhibitors. Thus, low-contrast gratings fitted to the lsRF or smaller are facilitatory, but high-contrast gratings fitted to the lsRF or larger are suppressive. Similarly, gratings engaging the far, but not the near, surround can facilitate the response to low contrast gratings fitted to the hsRF, but are suppressive when the contrast of the central grating is increased.

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What has emerged is the concept that the response of V1 neurons even to simple spatial patterns, such as gratings or bars, is the result of integration of inputs from FF, lateral and FB connections.

Kkoniocellular or interlaminar

Acknowledgments

This work was supported by grants from the National Science Foundation (IBN 0344569, and DMS 0515725), the National Eye Institute (EY 015262 and EY 015609), the Wellcome Trust (061113), the University of Utah Research Foundation and by a grant from Research to Prevent Blindness, Inc., New York, NY, to the Department of Ophthalmology, University of Utah, UT.

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