Contextual modulation in V1: the Rossi-Zipser controversy

Abstract

A recent study (Rossi et al. 2001) implied the absence of figure-ground based contextual modulation in macaque V1, in contrast to the study on which it was modelled (Zipser et al. 1996). We suggest that Rossi et al. may have underestimated the extent of modulation by considering only positive and not also negative modulation and that their data may have shown figure-ground based contextual modulation. We then suggest a paradigm to assess whether it reflects figure-ground segregation, boundaries, or both.

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Fig. 1A–C
Fig. 2

Notes

  1. 1.

    Albright and Stoner stated on p. 351: “... a more recent study (Rossi et al. 2001) failed to find any response differential in V1 for figure versus ground elements ...”

    Hochstein and Ahissar stated on p. 801: “Newer studies failed to replicate V1 figure-ground dependence, ... (Rossi et al. 2001).”

    Paradiso stated on p. 156: “... a more recent study has questioned [V1 responses consistent with figure-ground segregation] (Rossi et al. 2001).”

    Walker et al. stated on p. 5,659: “Regarding contextual effects in primary visual cortex, results of a recent study suggest that V1 neurons do not segregate figures from ground (Rossi et al. 2001).”

  2. 2.

    Zipser et al. stated on p. 7,383: “Extra-RF modulation declines monotonically with disc diameter reaching the value 1.0 at ~10° diameter.”

    Zipser et al. stated on p. 7,383: “The fraction of modulated sites reaches chance level at ~8° diameter.”

  3. 3.

    Rossi et al. stated on p. 1,701: “... using an orientation-defined figure with a diameter of 3°. This size was chosen to be beyond the range of significant contextual modulation effects ...”

    Rossi et al. stated on p. 1,702: “In the experiments described thus far, contextual modulation was observed only under conditions in which the figure diameters were 2° or less (...), ...”.

  4. 4.

    Rossi et al. stated on p. 1,701: “The mean of the distribution was significantly >1.0 for those stimulus conditions in which the orientation-defined figure was 1 or 2° in diameter (one-tailed t-test, p<0.05). For figure sizes >2°, the modulation index was approximately normally distributed around a value of 1.0.”

    Rossi et al. stated on p. 1,705: “The response modulation observed in V2 was similar to that observed in V1 in several ways. First, the mean modulation index was significantly >1.0 for orientation-defined figures having a diameter of 1 or 2°, but not for figures with diameters >2° (one-tailed t-test, p<0.05).”

    Their Fig. 3 and Table 2, displaying the mean modulation index for V1 and V2, respectively, indicated (asterisks) that the mean of the distribution was significantly >1.0 (one-tailed t-test, p<0.05) for figure sizes of 1°–2°, but not 3°–5°.

  5. 5.

    Rossi et al. stated on p. 1,704: “Regardless of the configuration of the stimulus, the percentage of our sample that showed a significant response to figure sizes of 4 and 5° was at, or close to, the percentage that would be expected to occur by chance (p=0.05, indicated by the arrow in Fig. 7B).”

  6. 6.

    Also Zipser et al. neglected negative modulation in that also they seem to consider that modulation exists only with an increase and not also with a decrease in spiking rate. Zipser et al. stated on p. 7,386: “In summary, when the RFs of V1 neurons appear to rest on a large flat textured surface (i.e. the homogeneous texture display), cells consistently give a small response, even when this surface is partially occluded by a frame [the frame display]. However, when the RFs of V1 neurons appear within a smaller “figure” surface surrounded by a moat [the moat display], consistent contextual modulation is evoked.” Zipser et al. stated on p. 7,385: “... the asymmetry in effect of moat and frame displays for evocation of extra-RF modulation ...”.

  7. 7.

    A problem with Fig. 6 was that figure sizes were not integers and that data was mixed for orientation-defined, luminance-defined, and color-defined figures; the first problem was solved by extrapolation and the second was ignored.

  8. 8.

    Zipser et al. seem to have used a different set of units for each of the four experiments, and although they give no information on the criterion for the selection of units in the second experiment investigating the spatial extent of modulation, they stated that they selected only about a third of the single units for the first experiment. Zipser et al. stated on p. 7,380: “The criterion for selecting a cell for experimentation [in the first experiment] was that it gave clear responses to at least one of the texture displays; this was the case with approximately one-third of the neurons that we isolated.” The rate of selection is therefore taken as 1/3.

  9. 9.

    Rossi et al. stated on p. 1,700: “We recorded from 135 sites in area V1 and 32 sites in area V2. Of these recording sites, we analyzed in detail 130 (V1, 73 single-unit and 29 multiunit; V2, 24 single-unit and 4 multiunit) that gave significant responses to the texture stimuli within the RF, were well isolated, and were held long enough to collect data for at least 20 presentations of each stimulus condition.” Also, Rossi et al. stated on p. 1,701: “Neurons [in V1] with RFs >1° (n=5) were excluded ...” They state thus very clearly as to why the number of V1 units decreased from 135 to 102 and then from 102 to 97. However, it is then less clear why the number of reported units was not 97 for every figure size, but instead 88/97/97/88/71 for a figure size of 1°/2°/3°/4°/5°, especially as Rossi et al. stated on p. 1,699: “Each neuron was tested with figure sizes from 1 to 5° in diameter,...”. The rate of selection is therefore taken as either 0.53 (71/135)–0.72 (97/135) or 0.76 (102/135).

  10. 10.

    Also other studies (Knierim and van Essen 1992; Jones et al. 2002) reported significant extra-CRF activation. However, the occurrence of extra-CRF activation seems to have led Rossi et al. to conclude that extra-CRF modulation did not occur (see first point) and/or that extra-CRF modulation reflected only boundaries (see second point).

    First, Rossi et al. stated in their Abstract: “For nearly all neurons (98/102), responses to a large texture figure did not differ from the responses to a uniform-texture background.” However, this does not seem correct: e.g. their Table 1 shows that for 19 neurons, the response to a 3° figure texture was significantly greater than to a uniform texture. This number (4/102) seems to correspond to their discussion of Table 1 on p. 1,705: “... fewer than five neurons [Table 1: 0–4 neurons] in our sample exhibited a significant degree of contextual modulation to the orientation-defined figure and did not respond to the surround texture alone.” (Possibly, their statement was intended to concern the nature rather than the existence of modulation, using ‘texture figure’ and ‘uniform-texture background’ as being critically different from ‘figure texture’ and ‘uniform background texture’, respectively, but even with such a use of word order, their statement seems premature, as suggested by the next point.)

    Second, Rossi et al. stated on p. 1,703: “That is, with a texture stimulus confined entirely to the surround, the presence of a texture boundary near the RF border elicited an excitatory response. This suggests ... that the location of the texture boundary within or near the RF was the most likely cause of the enhancement observed in the response to the orientation-defined figure described in the previous section.” However, this may be a premature conclusion. Indeed, modulation and activation, and thus their comparison, involve several possible effects: modulation involves (1) orientation of surround elements, and presence of (2) figure-ground and (3) boundary from orientation of elements; activation involves (1) presence of surround elements, and presence of (2) figure-ground and (3) boundary from presence of elements. Note hereby that Rossi et al. did not use complementary pairs of stimuli. Moreover, it seems difficult for an excitatory boundary effect to account not only for positive but also for negative modulation.

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Acknowledgements

We appreciate that the reviewing editor and referee were more receptive to the hypothesized relevance of negative modulation than previous reviewers.

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Correspondence to E. Corthout.

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EC and HS were supported by a NWO Cognition Program Grant

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Corthout, E., Supèr, H. Contextual modulation in V1: the Rossi-Zipser controversy. Exp Brain Res 156, 118–123 (2004). https://doi.org/10.1007/s00221-004-1847-8

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Keywords

  • Contextual modulation
  • Figure-ground segregation
  • Macaque
  • V1
  • Vision