J Physiol 589.12 (2011) pp 2921–2922 2921

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PERSPECT IVES

A new angle on the roleof feedfoward inputs in thegeneration of orientationselectivity in primary visualcortex

Luis M. MartinezInstituto de Neurociencias de Alicante,CSIC-Universidad Miguel Hernandez,Avenida Ramon y Cajal S/N, 03550 SantJoan d’Alacant, Spain

Email: l.martinez@umh.es

Fifty years ago, in this journal, Hubel& Wiesel (1962) published what hasbecome, arguably, one of the mostinfluential articles in systems neuro-science history. Inspired by a systematiccomparison of receptive field (RF) structurein thalamus (lateral geniculate nucleus,LGN) and primary visual cortex (V1),they described how V1 neurons couldbecome selective to the orientation of visualcontours, a critical first step towards objectrecognition.

Hubel and Wiesel’s model considers thatsimple cells and complex cells, the twomain RF classes they originally describedin V1, correspond to two successive stagesin cortical processing. In the first stage,simple cells could emerge in layer 4 fromthe convergence of thalamic inputs with

Figure 1. Two alternative feedforward models of the simple receptive fieldA, in Hubel and Wiesel’s original formulation, simple RFs (top) are generated in layer 4 from theconvergent input of On- and Off-centre geniculate neurons with RFs precisely arranged alongparallel rows in visual space (bottom). B, the new version of the feedforward model predictsthat rather than being aligned in rows, geniculate RFs overlap extensively in visual space(bottom); when linearly combined (middle), they generate population RFs that closely resemblethe structure and orientation selectivity of their targets in cortical layer 4 (top).

RFs arranged along a row in visual space.The spatial structure of the simple RF wouldthus represent the most parsimoniousapproach to build orientation detectorsdirectly from LGN cells with circular RFs(Fig. 1A).

Hubel and Wiesel’s hierarchical model,appealing for its simplicity and explanatorypower, did for systems neuroscience whatHodgkin and Huxley’s model of actionpotential generation had done for cellularneuroscience a couple of decades previously.Unlike Hodgkin and Huxley, however,Hubel and Wiesel were not at all precisein the mathematical formulation of theirproposal and the emergence of orientationselectivity has remained highly controversialever since.

In favour of a hierarchical model, it wasrecently found that cells with simple RFsare confined to regions that receive directthalamic inputs. In addition, it was reportedthat the RFs of LGN afferents are distributedin visual space along the preferred angleof a cortical orientation column, wherethey overlap the simple cell subregionsaccording to contrast sign and retinotopy(see Hirsch & Martinez (2006) for review).And finally, when the firing of corticalneurons is abolished, the spatial structureof the simple RF remains largely constantand the remaining (presumably thalamic)input to layer 4 simple cells appears to be

equally tuned for orientation (see Kara et al.(2002) for discussion).

Critiques to the hierarchical model, on theother hand, have mounted over the years.Some studies have even questioned theexistence of two discrete cell classes in V1,suggesting that Hubel and Wiesel’s simpleand complex cells represent the two endsof a continuum of receptive field structuresfound in all cortical layers. In addition,simple feedforward models cannot easilyaccount for various aspects of corticalresponses, such as the contrast invariance oforientation selectivity. Finally, only a smallfraction of the excitatory synapses in layer4 are made by feedforward LGN afferents.These results were used to promote the viewthat the thalamic input cannot by itselfdetermine the orientation selectivity, letalone other functional response properties,of cells in cortical layer 4. Therefore,several alternatives to the hierarchicalmodel, the so-called feedback models,have emerged which consider that thecortical microcircuit plays the crucial roleof amplifying and transforming the LGNinput according to context and behaviouralstate (see Hirsch & Martinez (2006) forreview).

To contribute even more to confoundthese two antagonistic paradigms, and thepundits, two recent reports (Jin et al.2011; Viswanathan et al. 2011, in a recentissue of The Journal of Physiology) nowargue against the thalamocortical patternof excitatory convergence implied in Hubeland Wiesel’s model. But, at the same time,they also suggest that orientation tuning atthe cortex must already be encoded in theresponse properties and partial segregationof On and Off cells in the LGN, aswas implicit in the original feedforwardhypothesis.

Jin et al. (2011) have found that thereceptive fields of On and Off LGN afferentsdo not always scatter along the preferredangle of a cortical orientation column.Instead, they overlap extensively and arerestricted to a small region of visualspace. However, when linearly combined,they generate spatial profiles resemblingthose of cortical simple cells and have thesame preferred orientation as the targetcortical column (Fig. 1B). In addition, ina recent issue of The Journal of Physiology,Viswanathan et al. (2011) used a clever

C© 2011 The Author. Journal compilation C© 2011 The Physiological Society DOI: 10.1113/jphysiol.2011.209031

2922 Perspectives J Physiol 589.12

variation of the approach of Kara et al.(2002) to isolate thalamic input to the cortexto show that the orientation selectivityseen in the subthreshold activity of simplecells during the silencing of cortical firingcould be explained by the orientationbiases in the output of single LGN cells,thus reducing the need for excitatoryconvergence from a long row of thalamicafferents.

Therefore, what is it going to be,feedforward or feedback, thalamocorticalor corticocortical? These recent reportshighlight that distinguishing betweenthese two antagonistic models of corticalorganization and function will require a full

understanding of how the thalamus trans-forms the retinal output before it reachesV1. We believe the computations performedat this subcortical nucleus will prove tobe fundamental, not only to explain thegeneration of orientation selectivity in catV1, but also to account for interspeciesdifferences in the emergence of corticalRFs and maps. If proved to be true, theconsequences will be far reaching, andmay bring us closer to understanding theemergence of much more complex RFstructures and cortical topography in areasdownstream of V1. Surprisingly, much canbe explained on purely feedforward groundsand without the need to invoke a complex

set of developmental wiring rules. A nicenew angle on an old riddle.

References

Hirsch J & Martinez LM (2006). Trends Neurosci29, 30–39.

Hubel DH & Wiesel TN (1962). J Physiol 160,106–154.

Jin J, Wang Y, Swadlow HA & Alonso J-M(2011). Nat Neurosci 14, 232–238.

Kara P, Pezaris JS, Yurgenson S & Reid RC(2002). Proc Natl Acad Sci U S A 99,16261–16266.

Viswanathan S, Jayakumar J & Vidyasagar TR(2011). J Physiol 589, 2349–2361.

C© 2011 The Author. Journal compilation C© 2011 The Physiological Society