Contrast gain control and horizontal interactions in V1: A DCM study

“For the analyses of this paper, we use those sites in the primary visual cortex that showed high sensitivity to the stimuli.”

“To address this relationship, we used dynamic causal modelling (DCM; Friston et al., 2003) to explain visually induced responses to stimuli of different contrast levels.”

“Bastos et al. (2012) compared the canonical microcircuit model from the Haeusler and Maass model to the theoretically-predicted circuit based on predictive coding(Friston,2008).”

“Lastly, in their revised model, dense (lateral) interconnections amongst the superficial pyramidal cells allow these cells to sample their diverse inputs on the dendritic tree and implement a version of a winner-take-all algorithm (Douglas and Martin, 2004).”

“These changes have been interpreted – in the context of predictive coding – as changes in the gain of superficial pyramidal cells reporting prediction error (Feldman and Friston, 2010).”

“Neural fi elds have a long and illustrious history in mathematical neuroscience, see Deco et al. (2008) and Nunez (1995) for a review.”

“Bastos et al. (2012) compared the canonical microcircuit model from the Haeusler and Maass model to the theoretically-predicted circuit based on predictive coding(Friston,2008).”

“A full description of these schemes can be found in Friston et al. (2007).”

“Whilst this core circuit has been established mostly for primary visual cortex (which is also our focus here), recent studies have also demonstrated that other cortical areas such as primary somatosensory and primary motor cortex share similar circuit properties (Lefort et al., 2009; Weiler et al., 2008).”

“…selective responses, we will see below that the use of a biophysically informed model allows us to infer that contrast dependent modulation of the effective spatial extent of neuronal connections contributes to the observed gamma response (a result that accords with single cell studies).”

“For example, Sceniak et al. (1999) recorded single units in V1 when monkeys fixated a point on the screen and were shown patches of drifting gratings at various contrasts and sizes.”

“This separates the sources of forward and backward connections in cortical hierarchies and has proved useful when trying to explain several aspects of distributed cortical computations in theoretical neurobiology (Bastos et al., 2012; Buffalo et al., 2011).”

“For example Thomson and Bannister (2003) combined multiple whole-cell recordings with histology to identify theprobabilityof fi ndinginterconnectedcellsbetweenparticularlayers, and their synaptic strengths.”

“Gamma band oscillations (30–100 Hz) in V1 are also sensitive to stimulus properties like contrast (and stimulus size) (Ray and Maunsell, 2010).”

“Contents lists available at ScienceDirect NeuroImage j ourna l homepage: www.e lsev ie r .com/ locate /yn img Contrast gain control and horizontal interactions in V1: A DCM study D.A. Pinotsis a,⁎, N. Brunet c,e, A. Bastos b,f, C.A. Bosman c,d, V. Litvak a, P. Fries b,c,1, K.J. Friston a,1 a The Wellcome Trust Centre…”

“Gamma band oscillations have been found to depend on neuronal interactions mediated by both gap junctions and synaptic transmission (Traub et al., 2001).”

“Whilst this core circuit has been established mostly for primary visual cortex (which is also our focus here), recent studies have also demonstrated that other cortical areas such as primary somatosensory and primary motor cortex share similar circuit properties (Lefort et al., 2009; Weiler et al., 2008).”

“The underlying assumption here is that the cortex acts as a dynamic fi lter of visual stimuli — that shows rapid nonlinear adaptation and where the local centre – surround interactions determine the frequency of gamma oscillations (Kapadia et al., 1999).”

“It is well-known that the local processing of information in the visual cortex is highly sensitive to the contrast of the stimuli being processed; see e.g. Sceniak et al. (2001, 2006).”

“For the analyses of this paper, we use those sites in the primary visual cortex that showed high sensitivity to the stimuli.”

“With increasing contrast, gamma oscillations increase in peak frequency (see also Roberts et al., 2013).”

“Haeusler and Maass used Hodgkin and Huxley neurons to build a realistic microcircuit model and showed that a cortical column – whose connectivity conforms to the canonical microcircuit – can perform various computations more efficiently, in relation to a column with random connectivity (Haeusler and Maass, 2007).”

“This model can generate differences in gamma responses that depend upon stimulus conditions that are thought to result from the interaction between local excitation and inhibition, (Brunel and Wang, 2003; Kang et al., 2010; Traub et al., 1997).”

“This is an important aspect of neural mass modelling of complex cross spectra in the time domain (see Friston et al 2012).”

“In the context of dynamic causal modelling, these quantities have been shown to accurately reflect neurotransmitter density and synaptic efficacy (Moran et al., 2008).”

“The advantage of neural fi eld models is that they can accommodate spatially extended activity on cortical manifold or patches that endows the predicted responses with a complicated frequency dependency (for a further discussion, see Pinotsis et al., 2012).”

“This separates the sources of forward and backward connections in cortical hierarchies and has proved useful when trying to explain several aspects of distributed cortical computations in theoretical neurobiology (Bastos et al., 2012; Buffalo et al., 2011).”

“This model can generate differences in gamma responses that depend upon stimulus conditions that are thought to result from the interaction between local excitation and inhibition, (Brunel and Wang, 2003; Kang et al., 2010;Traubetal.,1997).”

“Examplesofmorerealisticdynamiccausalmodellinginthiscontext can be found in Marreiros et al. (2010) and Pinotsis et al. (2013b).”

“It is well-known that the local processing of information in the visual cortex is highly sensitive to the contrast of the stimuli being processed; see e.g. Sceniak et al. (2001, 2006).”

“Examplesofmorerealisticdynamiccausalmodellinginthiscontext can be found in Marreiros et al. (2010) and Pinotsis et al. (2013b).”

“Our data suggest that there was no induced gamma peak for the two lowest contrasts and the corresponding spectra were rather featureless: but see also (Maris et al., 2013).”

“This is a ubiquitous choice in the neural fi eld literature, motivated by the sparse (heavy tailed) distribution of horizontal connections in sensory cortices: for more details, see (Baker and Cowan, 2009).”

“Examplesofmorerealisticdynamiccausalmodellinginthiscontext can be found in Marreiros et al. (2010) and Pinotsis et al. (2013b).”

“…attention (Auksztulewicz & Friston, 2015; Bauer, Stenner, Friston, & Dolan, 2014; Brown, Adams, Parees, Edwards, & Friston, 2013; Kanai, Komura, Shipp, & Friston, 2015; Pinotsis et al., 2014); namely, a precision engineered gain control of prediction error units (i.e., superficial pyramidal cells).”

“In addition, computational modeling studies have shown the plausibility of superficial gamma circuits to engage in prediction error computations (38, 41, 42).”

“These relationships have been examined using Bayesian model comparison of dynamic causal models that embody competing hypotheses about how visual contrast effects lateral interactions [32].”

“, 2013) and ECoG within-area cross-spectral densities (Pinotsis et al., 2014).”

“, by targeting inhibitory interneurons that are coupled to the superficial pyramidal cells broadcasting prediction errors [78, 79].”

“, 2003) as well as electrophysiology (Bastos et al., 2015a; Friston et al., 2012; Pinotsis et al., 2014).”

“Given the prominence of NMDA-Rs in superficial cortical layers, it is unsurprising that the gain of superficial pyramidal cell populations is strongly affected by NMDAR function [Fox et al., 1990; Pinotsis et al., 2014].”

“This interpretation appears to have a degree of validity in relation to attentional gain and enjoys the support of several empirical studies (e.g., Fogelson et al., 2014; Pinotsis et al., 2014; Auksztulewicz and Friston, 2015; Vossel et al., 2015).”

“The ephaptic model isusedtwicebelow:first,in“Methods,”toderivethemathematical expression of ephaptic coupling and then, in “Results,” to find evidence of ephaptic coupling using BMC.”

“…, including working memory (Miller et al., 2018; Pinotsis et al., 2018), attention (Fiebelkorn and Kastner, 2019; Buschman and Miller, 2007; Lakatos et al., 2008; Pinotsis et al., 2014; Fries et al., 2001; Gregoriou et al., 2009), and predictive coding (Bastos et al., 2020; Pinotsis et al., 2017b).”

“This process has also been described in detail in several earlier publications (Friston et al. 2012; Pinotsis et al. 2014).”

“Indeed the CMC used here is based upon the model and populations in (22, 23, 32, 34, 36, 62), differing only in the local coupling among populations.”

“These cell populations are the sources of forward and backward extrinsic (betweensource) connections respectively (Pinotsis et al., 2014).”

“…why superficial pyramidal cells have so many synaptic gain control mechanisms (NMDA receptors, D1 dopamine receptors, etc.), in order to set the gain or precision of prediction errors—thought to be encoded by superficial pyramidal cells (Pinotsis et al., 2014; Kanai et al., 2015; Shipp, 2016).”

“In this setting, laminar LFP responses y i – of the sort measured with multi-electrode shanks – are generated by contributions from excitatory and inhibitory populations that occupy one or more cortical layers, see also (Pinotsis et al., 2012b, 2014).”

“The effects of contrast on the induced rhythms are complex and specifically influence the postsynaptic gain of neuronal populations, the strength of intrinsic and horizontal connectivity which can be differentially engaged depending on stimulus properties (Pinotsis et al., 2014).”

“Pinotsis et al. (2014) were able to reproduce stimulus contrast dependences in neuronal responses and track their origins to the pyramidal neurons with forward projections.”

“Crucially, synaptic gain is parameterized as the intrinsic—or self-inhibitory— connectivity of superficial pyramidal cell populations in DCM [Bastos et al., 2012; Friston, 2008; Pinotsis et al., 2014; Stephan et al., 2006].”

“, 2012; Alitto and Usrey, 2008], which optimize the precision or gain of units encoding visual prediction errors: see [Pinotsis et al., 2014] for a discussion of the role of gain and precision in contrast effects.”

“Recent modelling has begun to identify some of the parameters which are critical in determining the contrast gain of gamma [38].”

“For the explicit form of the transfer functions T ð k ; x ; h ð 1 Þ Þ we refer the interested reader to (Pinotsis et al. 2014).”

“There are also several examples in the literature that use dynamic causal modelling to disambiguate between inhibitory and excitatory connections in cortical hierarchies [35–41].”

“This experimental study alongwith other recent works by Bastos et al. (2012) and Pinotsis et al. (2014) suggest that the non-local inhibitory neurons implicitly behave as an effective negative feedback to excitatory cell populations.”

“, prediction errors) is thought to be mediated by intrinsic excitability (or self-inhibition; Bhatt et al., 2016; Brown & Friston, 2012; Pinotsis et al., 2014).”

“…of in terms of the precision of prediction errors, i.e., an estimate of predictability ( Ainley et al., 2016 ; Auksztulewicz and Friston, 2016 ; FitzGerald et al., 2015 ; Haarsma et al., 2020 ; Kok et al., 2012 ; Pinotsis et al., 2014 ; Shipp, 2016 ; Spratling, 2017 ; Sterzer et al., 2018 ).”

“These can be accommodated by using the effective connectivity parameters obtained here as priors to fit a more complicated biophysical model that accounts for volume conduction effects (Pinotsis et al., 2014).”

“In our second study [10], neuronal signals were recorded while a monkey first fixated its gaze (in a window with 1 radius) and later released a lever when it detected a color change at fixation.”

“The data analyzed here have been (partially) used in previous studies (15, 18, 19, 22, 33, 54-59).”

“In our first study [5], we exploited high density spatially resolved data from multielectrode electrocorticographic (ECoG) arrays to study the effect of varying stimulus contrast on cortical excitability and gamma peak frequency.”

“…prediction errors being passed from a lower to a higher area, whereas inhibitory effective connectivity re fl ects the explaining away (reduced excitation) of the prediction error lower in the hierarchy, generally thought to be mediated by inhibitory inter-neurons within the target region 33 – 36 .”

“For the estimation of effective connections between the dlPFC and pre-SMA underlying the changes reported above, we applied DCM for cross-spectral density based on the canonical microcircuit model (CMC; [56, 57].”

“This interesting compromise between biological significance and abstraction explains the wide range of neural fields applications, which cover primary visual cortex [3, 37], auditory system [6], working memory [31], sensory cortex [21], and deep brain structures involved in Parkinson’s disease [14].”

“Population-level modeling studies have proposed that ɣ synchronization relates to the gain of superficial pyramidal neurons ( 20 , 69 , 70 ) ; through the lens of predictive processing, ɣ oscillations may regulate feedforward prediction-error signaling ( 12 , 20 , 21 ) .”

“In this and subsequent figures, precision weighted prediction errors are denoted by ξ =  ε = ε − ξ , were  is a precision matrix and  can be regarded as the strength of horizontal connections (Pinotsis et al., 2014; Tang et al., 2023).”

“Physiologically, the corresponding precision or postsynaptic gain control is generally thought to be mediated by neuromodulatory mechanisms of various sorts (Limanowski 2022; Pinotsis et al. 2014; Vossel et al. 2015).”