Castaldi, Elisa

Cicchini, Guido Marco

Morrone, Maria Concetta

Tinelli, Francesca

English

Archivio della Ricerca - Università di Pisa

Full Terms & Conditions of access and use can be found athttps://www.tandfonline.com/action/journalInformation?journalCode=pcgn20Cognitive NeuropsychologyISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/pcgn20Does more imply better vision?Elisa Castaldi, Guido Marco Cicchini, Francesca Tinelli & Maria ConcettaMorroneTo cite this article: Elisa Castaldi, Guido Marco Cicchini, Francesca Tinelli & MariaConcetta Morrone (2022): Does more imply better vision?, Cognitive Neuropsychology, DOI:10.1080/02643294.2022.2052715To link to this article:  https://doi.org/10.1080/02643294.2022.2052715© 2022 The Author(s). Published by InformaUK Limited, trading as Taylor & FrancisGroupPublished online: 25 Mar 2022.Submit your article to this journal Article views: 448View related articles View Crossmark dataARTICLE COMMENTARYDoes more imply better vision?Elisa Castaldi a, Guido Marco Cicchinib, Francesca Tinellic and Maria Concetta Morronec,daDepartment of Neuroscience, Psychology, Pharmacology and Child Health, University of Florence, Florence, Italy; bInstitute of Neuroscience,National Research Council (CNR), Pisa, Italy; cScientific Institute Stella Maris (IRCSS), Pisa, Italy; dDepartment of Translational Research on NewTechnologies in Medicine and Surgery, University of Pisa, Pisa, ItalyARTICLE HISTORY Received 15 November 2021; Revised 8 February 2022; Accepted 8 March 2022Correctly identifying the orientation of objects inspace is crucial in many aspects of our life, fromdaily activities requiring efficient tool use to geometri-cal learning.Vannuscorps et al. (2021), in the current issue,finely characterize the interesting case of a woman,Davida, who fails to recognize orientation. Davida, ateenager with a normal medical history, no evidenceof cortical abnormalities, and proficient in manyvisual tasks, performs poorly when she has toprocess visually the orientation of high contrast 2Dshapes. Davida, however, performs perfectly whenshe is asked to recognize items haptically. Theauthors interpreted this pattern of deficits as the con-sequence of an impairment at an intermediate stageof processing from a pure retinotopic frame of refer-ence to a complete spatiotopic representation ofspace that is independent of our body/gaze direction.The authors refer to this intermediate level as an“intermediate shape-centred representation” (ISCRs)that should correspond to an allocentric frame ofreference (centred on the visual object). A largebody of literature demonstrates that the brain simul-taneously uses many frames of reference (Cohen &Andersen, 2002; Goodale, 2014), and the fact thatonly one frame can be affected in an otherwisetypical woman strongly corroborates the idea of mul-tiple representations, showing the complexity and thefragility of the mechanisms which generate spacerepresentation.Davida’s impairments are consistent with damageat an early stage along the cortical visual pathwaysin contrast to earlier studies that demonstrateddamage at a higher tier of multimodal cortical proces-sing (Castaldi et al., 2018; Goodale, 2014). We haverecently described a group of children with lesionsat the level of the periventricular white matter (PVL)that presented agnosia for mirror orientation thatwas specific only for diagonal orientations (Castaldiet al., 2018). They consistently confused diagonalorientations with their mirror counterpart, while per-ception of cardinal orientations was preserved. Thedeficit generalized to stimuli varying in many low-level features, such as oriented gratings or bars orsecond order stimuli (i.e., collinear short linesembedded within randomly oriented lines) and alsoaffected the haptic modality. The selectivity of theirdeficit for diagonal orientations allowed us to testthe specificity of this deficit for retinotopic vs. spatio-topic frame of reference and we demonstrated thatthe visual orientation deficit remained selective forthe diagonal orientations in space, indicating thatthe effect occurred in spatiotopic and not retinotopiccoordinates and that it was independent of gravityand of the monitor frame of reference (allocentric rep-resentation). One of implications of the deficitsdescribed in our PVL patients is that perception ofvisual orientation of oblique and cardinal stimulusrelies on partially separate mechanisms. In thisrespect it would be interesting to test Davida alsowith oblique orientations in those conditions thatyield high performance with cardinal orientations(e.g., low contrast).Perception of object orientation in space isachieved through a cascade of visual processingsteps, the first of which consists of the identification© 2022 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis GroupThis is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or builtupon in any way.CONTACT Elisa Castaldi elisa.castaldi@unifi.it Via di San Salvi 12, Florence, 50135, ItalyCOGNITIVE NEUROPSYCHOLOGYhttps://doi.org/10.1080/02643294.2022.2052715of 2D edges and lines allowing for detection and seg-regation of the objects’ borders from the background(Burr et al., 1989, 1992; Morrone & Burr, 1988). There isevidence that the identification and discrimination ofedges and lines is supported by regions along boththe ventral (V4) and the dorsal stream (caudal partof the intraparietal sulcus, transversal occipitalsulcus, dorsal LO and V3A), irrespective of these fea-tures being defined by luminance or chromatic con-trast (Castaldi et al., 2013; Perna et al., 2005, 2008).Areas along the dorsal pathway presumably startfrom this local information and compute objects’orientation independently of retinotopic coordinatesand even irrespective of the modality, visual ortactile (Kitada et al., 2006), to support action guidance(Goodale, 2014). In the light of this evidence, it is likelythat the deficit observed in our PVL patients arisesfrom a lesion of the posterior parietal cortex, whichis often reported to be damaged in this pathology(Fiori et al., 2015) and is consistent with their deficitbeing invariant to spatiotopic coordinates.The case study of Davida, clearly different from ourPVL children, probably occurred at an earlier stage ofvisual analysis, her dependence on contrast of the orien-tation deficit strongly supporting this view. She showedsmall deficits or none at all when the oriented stimuliwere blurred or defined by small dots, or lines, or hadlow contrast (i.e., with low energy stimuli). To interpretthese findings, the authors suggested the formationalong the extrastriate pathways of multiple indepen-dent “intermediate shape-centred representations”(ISCRs) associated with the different visual cues (likecolour, luminance, low contrast, high contrast, etc).However, simpler explanations are equally poss-ible. High contrast stimuli do not always lead tobetter perception and Davida is not the only patientshowing consistent deficits only at high contrast.Tadin’s work (2003, 2015) has shown a significantdrop in performance for high contrast motionstimuli and we demonstrated it in typical participantsas well as those with dyslexia (Bhat et al., 2018; Peraniet al., 2021). In Perani et al. (2021) discrimination per-formance topped between 10% and 30% Michelsoncontrast and then, surprisingly, dropped at highercontrast, in particular in a subgroup of dyslexic indi-viduals carrying a specific genetic variant (theDCDC2 gene deletion). Interestingly, motion contrastsensitivity and high contrast accuracy in these individ-uals correlated with the fractional anisotropy in theoptic radiations and ventral tracts located in theinferior temporal cortex (inferior longitudinal andinferior fronto-occipital fasciculi), which provideinput/output to V1. These deficits are stronger athigh spatial frequency stimuli (see Fig 1G&H inPerani et al., 2021), and this is consistent withDavida’s perception showing stronger deficits forobjects defined by sharp edges. Also, the apparentlynormal perception that Davida displays in Experiment5.9, 5.10 and 6.10 is consistent with the hypothesisthat high contrast explains the deficit: despite thehigh contrast of the single dots or pixels, the lowdensity of dots or pixels defining either the shapesor the motion in those paradigms reduce dramaticallythe effective contrast of the stimuli after accountingfor the small blurring associated with normal acuity.One possible explanation for these and Davida’scontrast-dependent deficits might be that contrastis correctly computed in V1, but then the read-outof this first stage by higher order areas (such as V4in the case of Davida) is impaired. Neural responsesto increasing luminance contrast levels are typicallydescribed by sigmoid-like functions, defined by amonotonic increase in neural firing with increasingcontrast up to a maximum saturation level (Albrecht& Hamilton, 1982). However, this pattern is notcommon to all neurons in all visual processingstages. For example, neurons in macaque area V4can display bandpass tuning response for contrast(Sani et al., 2013) during an orientation discriminationtask. Interestingly the non-monotonic U-shapedselectivity emerged only later in the neuronalresponse (at around 150 ms after stimulus onset)suggesting a longer integration time. Sani et al.(2013) proposed that contrast should be consideredan independent and basic feature, such as color ororientation, and that the slower non-monotonictype of response might correspond to a contrast cat-egorization stage. Psychophysical studies seem tosupport the existence of contrast selective neuronsin humans as well, by showing that adapting to a con-trast defined (2nd order) pattern of fixed contrastimpairs the visibility of test patterns composed ofelements with straddling contrast (Wolfson &Graham, 2007, 2009). These are hallmarks of asensory domain which represents contrast flexibly.In the light of these results, it would be interestingto test Davida with a similar contrast adaptation para-digm to evaluate whether some of these channels2 E. CASTALDI ET AL.coding for medium to high contrast are impaired andcause the reported orientation deficit.Disclosure statementNo potential conflict of interest was reported by the author(s).FundingThis research was funded by the European Research Council—grant agreement no. 832813—ERC Advanced “Spatio-tem-poral mechanisms of generative perception—GenPercept”;from Flag-ERA JTC 2019 (grant DOMINO); and from Italian Min-istry of Education, University, and Research under thePRIN2017 program (grant number 2017SBCPZY—“Temporalcontext in perception: serial dependence and rhythmicoscillations”).ORCIDElisa Castaldi http://orcid.org/0000-0003-0327-6697ReferencesAlbrecht, D. G., & Hamilton, D. B. (1982). Striate cortex ofmonkey and cat: Contrast response function. Journal ofNeurophysiology, 48(1), 217–237. https://doi.org/10.1152/jn.1982.48.1.217Bhat, A., Cicchini, G. M., & Burr, D. C. (2018). Inhibitory sur-rounds of motion mechanisms revealed by continuoustracking. 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Does more imply better vision?

Castaldi, E.

Cicchini, G. M.

Tinelli, F.

Morrone, M. C.

Florence Research

https://flore.unifi.it/bitstream/2158/1274407/1/2022%20Castaldi%20et%20al%20Cog%20Neur.pdf

Does more imply better vision?

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