A Papanikolaou

A new method for estimating population receptive field topography in visual cortex

We introduce a new method for measuring visual population receptive fields (pRF) with functional magnetic resonance imaging (fMRI). The pRF structure is modeled as a set of weights that can be estimated by solving a linear model that predicts the Blood Oxygen Level-Dependent (BOLD) signal using the stimulus protocol and the canonical hemodynamic response function. This method does not make a priori assumptions about the specific pRF shape and is therefore a useful tool for uncovering the underlying pRF structure at different spatial locations in an unbiased way. We show that our method is more accurate than a previously described method (Dumoulin and Wandell, 2008) which directly fits a 2-dimensional isotropic Gaussian pRF model to predict the fMRI time-series. We demonstrate that direct-fit models do not fully capture the actual pRF shape, and can be prone to pRF center mislocalization when the pRF is located near the border of the stimulus space. A quantitative comparison demonstrates that our method outperforms the direct-fit methods in the pRF center modeling by achieving higher explained variance of the BOLD signal. This was true for direct-fit isotropic Gaussian, anisotropic Gaussian, and difference of isotropic Gaussians model. Importantly, our model is also capable of exploring a variety of pRF properties such as surround suppression, receptive field center elongation, orientation, location and size. Additionally, the proposed method is particularly attractive for monitoring pRF properties in the visual areas of subjects with lesions of the visual pathways, where it is difficult to anticipate what shape the reorganized pRF might take. Finally, the method proposed here is more efficient in computation time than direct-fit methods, which need to search for a set of parameters in an extremely large searching space. Instead, this method uses the pRF topography to constrain the space that needs to be searched for the subsequent modeling.

Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects

Significance Partial damage of the primary visual cortex (V1), or damage to the white matter inputs to V1 (optic radiation), cause blindness in specific regions of the visual field. We use functional MRI to measure responses in individual patients with a localized, chronic V1 injury that resulted in blindness in a quarter of the visual field. The fMRI responses of patients and controls are generally similar, but in some patients differences from controls can be measured. Importantly, responses in spared early visual cortex are not always congruent with visual perception. Understanding how the properties of early visual areas respond to injury will lead to better strategies for visual rehabilitation. Injury to the primary visual cortex (V1) typically leads to loss of conscious vision in the corresponding, homonymous region of the contralateral visual hemifield (scotoma). Several studies suggest that V1 is highly plastic after injury to the visual pathways, whereas others have called this conclusion into question. We used functional magnetic resonance imaging (fMRI) to measure area V1 population receptive field (pRF) properties in five patients with partial or complete quadrantic visual field loss as a result of partial V1+ or optic radiation lesions. Comparisons were made with healthy controls deprived of visual stimulation in one quadrant [“artificial scotoma” (AS)]. We observed no large-scale changes in spared-V1 topography as the V1/V2 border remained stable, and pRF eccentricity versus cortical-distance plots were similar to those of controls. Interestingly, three observations suggest limited reorganization: (i) the distribution of pRF centers in spared-V1 was shifted slightly toward the scotoma border in 2 of 5 patients compared with AS controls; (ii) pRF size in spared-V1 was slightly increased in patients near the scotoma border; and (iii) pRF size in the contralesional hemisphere was slightly increased compared with AS controls. Importantly, pRF measurements yield information about the functional properties of spared-V1 cortex not provided by standard perimetry mapping. In three patients, spared-V1 pRF maps overlapped significantly with dense regions of the perimetric scotoma, suggesting that pRF analysis may help identify visual field locations amenable to rehabilitation. Conversely, in the remaining two patients, spared-V1 pRF maps failed to cover sighted locations in the perimetric map, indicating the existence of V1-bypassing pathways able to mediate useful vision.

Visual cortex organisation in a macaque monkey with macular degeneration

The visual field is retinotopically represented in early visual areas. It has been suggested that when adult primary visual cortex (V1) is deprived of normal retinal input it is capable of large‐scale reorganisation, with neurons inside the lesion projection zone (LPZ) being visually driven by inputs from intact retinal regions. Early functional magnetic resonance imaging (fMRI) studies in humans with macular degeneration (MD) report > 1 cm spread of activity inside the LPZ border, whereas recent results report no shift of the LPZ border. Here, we used fMRI population receptive field measurements to study, for the first time, the visual cortex organisation of one macaque monkey with MD and to compare it with normal controls. Our results showed that the border of the V1 LPZ remained stable, suggesting that the deafferented area V1 zone of the MD animal has limited capacity for reorganisation. Interestingly, the pRF size of non‐deafferented V1 voxels increased slightly (~20% on average), although this effect appears weaker than that in previous single‐unit recording reports. Area V2 also showed limited reorganisation. Remarkably, area V5/MT of the MD animal showed extensive activation compared to controls stimulated over the part of the visual field that was spared in the MD animal. Furthermore, population receptive field size distributions differed markedly in area V5/MT of the MD animal. Taken together, these results suggest that V5/MT has a higher potential for reorganisation after MD than earlier visual cortex.

Differential neural mechanisms for early and late prediction error detection

Emerging evidence indicates that prediction, instantiated at different perceptual levels, facilitate visual processing and enable prompt and appropriate reactions. Until now, the mechanisms underlying the effect of predictive coding at different stages of visual processing have still remained unclear. Here, we aimed to investigate early and late processing of spatial prediction violation by performing combined recordings of saccadic eye movements and fast event-related fMRI during a continuous visual detection task. Psychophysical reverse correlation analysis revealed that the degree of mismatch between current perceptual input and prior expectations is mainly processed at late rather than early stage, which is instead responsible for fast but general prediction error detection. Furthermore, our results suggest that conscious late detection of deviant stimuli is elicited by the assessment of prediction error’s extent more than by prediction error per se. Functional MRI and functional connectivity data analyses indicated that higher-level brain systems interactions modulate conscious detection of prediction error through top-down processes for the analysis of its representational content, and possibly regulate subsequent adaptation of predictive models. Overall, our experimental paradigm allowed to dissect explicit from implicit behavioral and neural responses to deviant stimuli in terms of their reliance on predictive models.

A Systematic Approach to Visual System Rehabilitation — Population Receptive Field Analysis and Real-time Functional Magnetic Resonance Imaging Neurofeedback Methods

Visual information transmission flows from the retinal ganglion cells to the lateral geniculate nucleus and then to the primary visual cortex (V1), the chief cortical relay of visual information and in turn, to “higher” extrastriate areas. Beyond area V1, visual processing is distributed across multiple interconnected brain areas, the precise role of which and their interactions are not yet, completely understood. To add to the dynamic complexity of the system, feedback from higher areas and modulation by top-down processes, such as attention are often critical in the formation of visual percepts (Deco and Lee; 2004; Olhausen, 2003; Kastner and Unger‐ leider, 2000; Mumford, 1994; Hubel and Weisel, 1977).

Nonlinear population receptive field changes in human area V5/MT+ of healthy subjects with simulated visual field scotomas.

There is extensive controversy over whether the adult visual cortex is able to reorganize following visual field loss (scotoma) as a result of retinal or cortical lesions. Functional magnetic resonance imaging (fMRI) methods provide a useful tool to study the aggregate receptive field properties and assess the capacity of the human visual cortex to reorganize following injury. However, these methods are prone to biases near the boundaries of the scotoma. Retinotopic changes resembling reorganization have been observed in the early visual cortex of normal subjects when the visual stimulus is masked to simulate retinal or cortical scotomas. It is not known how the receptive fields of higher visual areas, like hV5/MT+, are affected by partial stimulus deprivation. We measured population receptive field (pRF) responses in human area V5/MT+ of 5 healthy participants under full stimulation and compared them with responses obtained from the same area while masking the left superior quadrant of the visual field (“artificial scotoma” or AS). We found that pRF estimations in area hV5/MT+ are nonlinearly affected by the AS. Specifically, pRF centers shift towards the AS, while the pRF amplitude increases and the pRF size decreases near the AS border. The observed pRF changes do not reflect reorganization but reveal important properties of normal visual processing under different test-stimulus conditions.

Topographical estimation of visual population receptive fields by FMRI.

Visual cortex is retinotopically organized so that neighboring populations of cells map to neighboring parts of the visual field. Functional magnetic resonance imaging allows us to estimate voxel-based population receptive fields (pRF), i.e., the part of the visual field that activates the cells within each voxel. Prior, direct, pRF estimation methods(1) suffer from certain limitations: 1) the pRF model is chosen a-priori and may not fully capture the actual pRF shape, and 2) pRF centers are prone to mislocalization near the border of the stimulus space. Here a new topographical pRF estimation method(2) is proposed that largely circumvents these limitations. A linear model is used to predict the Blood Oxygen Level-Dependent (BOLD) signal by convolving the linear response of the pRF to the visual stimulus with the canonical hemodynamic response function. PRF topography is represented as a weight vector whose components represent the strength of the aggregate response of voxel neurons to stimuli presented at different visual field locations. The resulting linear equations can be solved for the pRF weight vector using ridge regression(3), yielding the pRF topography. A pRF model that is matched to the estimated topography can then be chosen post-hoc, thereby improving the estimates of pRF parameters such as pRF-center location, pRF orientation, size, etc. Having the pRF topography available also allows the visual verification of pRF parameter estimates allowing the extraction of various pRF properties without having to make a-priori assumptions about the pRF structure. This approach promises to be particularly useful for investigating the pRF organization of patients with disorders of the visual system.

Measuring single neuron visual receptive field sizes by fMRI

The non-invasive measurements of neuronal receptive field (RF) properties in-vivo allow a detailed understanding of brain organization as well as its plasticity by longitudinal following of potential changes. Visual RFs measured invasively by electrophysiology in animal models have traditionally provided a great extent of our current knowledge about the visual brain and its disorders. Voxel based estimates of population RF (pRF) by functional magnetic resonance imaging (fMRI) in humans revolutionized the field and have been used extensively in numerous studies. However, current methods cannot estimate single-neuron RF sizes as they reflect large populations of neurons with individual RF scatter. Here, we introduce a new approach to estimate RF size using spatial frequency selectivity to checkerboard patterns. This method allowed us to obtain non-invasive, single-unit, RF estimates in human V1 for the first time. These estimates were significantly smaller compared to prior pRF methods. Further, fMRI and electrophysiological experiments in non-human primates demonstrated an exceptional match validating the approach.

Organization of area hV5/MT+ in subjects with homonymous visual field defects

ABSTRACT Damage to the primary visual cortex (V1) leads to a visual field loss (scotoma) in the retinotopically corresponding part of the visual field. Nonetheless, a small amount of residual visual sensitivity persists within the blind field. This residual capacity has been linked to activity observed in the middle temporal area complex (V5/MT+). However, it remains unknown whether the organization of hV5/MT+ changes following early visual cortical lesions. We studied the organization of area hV5/MT+ of five patients with dense homonymous defects in a quadrant of the visual field as a result of partial V1+ or optic radiation lesions. To do so, we developed a new method, which models the boundaries of population receptive fields directly from the BOLD signal of each voxel in the visual cortex. We found responses in hV5/MT+ arising inside the scotoma for all patients and identified two possible sources of activation: 1) responses might originate from partially lesioned parts of area V1 corresponding to the scotoma, and 2) responses can also originate independent of area V1 input suggesting the existence of functional V1‐bypassing pathways. Apparently, visually driven activity observed in hV5/MT+ is not sufficient to mediate conscious vision. More surprisingly, visually driven activity in corresponding regions of V1 and early extrastriate areas including hV5/MT+ did not guarantee visual perception in the group of patients with post‐geniculate lesions that we examined. This suggests that the fine coordination of visual activity patterns across visual areas may be an important determinant of whether visual perception persists following visual cortical lesions. HighlightsWe studied hV5/MT+ responses in patients with early visual cortical damage.We developed a new population receptive field measurement method.We found responses in hV5/MT+ arising inside the scotoma for all patients.Responses in hV5/MT+ originate either from V1 or from V1‐bypassing pathways.Activity in either V1 and/or hV5/MT+ is not sufficient to mediate conscious vision.

Erratum: Corrigendum: Differential neural mechanisms for early and late prediction error detection

Scientific Reports 6: Article number: 24350; published online: 15 April 2016; updated: 11 April 2017 In this Article, an additional affiliation for Paul F.M.J. Verschure was omitted. The correct affiliations for Paul F.M.J. Verschure are listed below: SPECS, Universitat Pompeu Fabra, Barcelona, Spain.