Towards a Unified View on Pathways and Functions of Neural Recurrent Processing
Authors: Cyriel M.A. Pennartz, Shirin Dora, Lars Muckli, Jeannette A.M. Lorteije
Journal: Trends in Neurosciences (2019)

Corticocortical feedback to V1 is likely to be involved in contextual modulation of stimulus processing, high-level information processing, and predictive processing.The pulvinar is proposed to act as a fast, short-cut connection between visual areas to accelerate predictive processing.Cholinergic projections could contribute to functions of recurrent processing, but the speed of recurrent processing from V1 to the basal forebrain and back is too low to modulate information processing at short latencies.A plausible anatomical mapping is proposed from a functional model of predictive processing onto cortical microcircuitry.Stimulus-context modulation and high-level information processing can be encapsulated in a predictive processing framework including feedforward and recurrent processing, if this is broadened to include the generation of interpretations and inferences on sensory inputs in general. There are three neural feedback pathways to the primary visual cortex (V1): corticocortical, pulvinocortical, and cholinergic. What are the respective functions of these three projections? Possible functions range from contextual modulation of stimulus processing and feedback of high-level information to predictive processing (PP). How are these functions subserved by different pathways and can they be integrated into an overarching theoretical framework? We propose that corticocortical and pulvinocortical connections are involved in all three functions, whereas the role of cholinergic projections is limited by their slow response to stimuli. PP provides a broad explanatory framework under which stimulus-context modulation and high-level processing are subsumed, involving multiple feedback pathways that provide mechanisms for inferring and interpreting what sensory inputs are about. There are three neural feedback pathways to the primary visual cortex (V1): corticocortical, pulvinocortical, and cholinergic. What are the respective functions of these three projections? Possible functions range from contextual modulation of stimulus processing and feedback of high-level information to predictive processing (PP). How are these functions subserved by different pathways and can they be integrated into an overarching theoretical framework? We propose that corticocortical and pulvinocortical connections are involved in all three functions, whereas the role of cholinergic projections is limited by their slow response to stimuli. PP provides a broad explanatory framework under which stimulus-context modulation and high-level processing are subsumed, involving multiple feedback pathways that provide mechanisms for inferring and interpreting what sensory inputs are about. Primary sensory cortical areas are the entry points for sensory information reaching the cortex. Sensory information arrives through thalamic projections, and after processing in primary areas information is forwarded to higher sensory and association cortices. In addition to engaging in feedforward processing [1.Serre T. et al.A feedforward architecture accounts for rapid categorization.Proc. Natl. Acad. Sci. U. S. A. 2007; 104: 6424-6429Crossref PubMed Scopus (0) Google Scholar], primary sensory cortices receive feedback from higher cortical areas and thus partake in recurrent processing (RP) (see Glossary) [2.Felleman D.J. Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex.Cereb. Cortex. 1991; 1: 1-47Crossref PubMed Google Scholar, 3.Markov N.T. et al.Anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex.J. Comp. Neurol. 2014; 522: 225-259Crossref PubMed Scopus (177) Google Scholar], which may serve multiple functions (Figure 1). Feedback reaches the primary sensory cortices through various anatomical pathways. Here we focus mainly on V1 and highlight three major pathways that have been identified in both primates and rodents (Figure 2 and Box 1). First, V1 receives reciprocal feedback projections from those visual cortices that it projects to, most notably areas V2, V3, and V4 [2.Felleman D.J. Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex.Cereb. Cortex. 1991; 1: 1-47Crossref PubMed Google Scholar] in primates and the lateromedial (LM) and posteromedial (PM) cortices in rodents [4.Glickfeld L.L. Olsen S.R. Higher-order areas of the mouse visual cortex.Annu. Rev. Vis. Sci. 2017; 3: 251-273Crossref PubMed Scopus (8) Google Scholar, 5.D'Souza R.D. et al.Recruitment of inhibition and excitation across mouse visual cortex depends on the hierarchy of interconnecting areas.eLife. 2016; 5e19332Crossref PubMed Scopus (12) Google Scholar], which we call short-range projections. Additionally, V1 receives input from higher cortical areas in the temporal, parietal, and frontal lobes [2.Felleman D.J. Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex.Cereb. Cortex. 1991; 1: 1-47Crossref PubMed Google Scholar]. These higher areas project to V1 along the same hierarchical routes (e.g., via V4 in primates [6.Moore T. Armstrong K.M. Selective gating of visual signals by microstimulation of frontal cortex.Nature. 2003; 421: 370-373Crossref PubMed Scopus (703) Google Scholar]) and in mice also through direct long-range projections [7.Zhang S. et al.Long-range and local circuits for top-down modulation of visual cortex processing.Science. 2014; 345: 660-665Crossref PubMed Scopus (202) Google Scholar]. Second, in the context of thalamic pathways, V1 receives not only feedforward projections from the lateral geniculate thalamic nucleus (LGN) but also feedback from the thalamic pulvinar region [8.Shipp S. The functional logic of cortico–pulvinar connections.Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2003; 358: 1605-1624Crossref PubMed Scopus (0) Google Scholar] [or its rodent homolog, the lateral posterior thalamic nucleus (LP)] [9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar]. Because the pulvinar receives projections from visual areas, higher cortical areas and subcortical structures including the amygdala and basal ganglia, its projections to V1 could convey a wide range of information, from stimulus context to cognitive content. Furthermore, pulvinar activity affects the processing of visual information in V1 [10.Purushothaman G. et al.Gating and control of primary visual cortex by pulvinar.Nat. Neurosci. 2012; 15: 905-912Crossref PubMed Scopus (95) Google Scholar] and V4 [11.Zhou H. et al.Pulvinar–cortex interactions in vision and attention.Neuron. 2016; 89: 209-220Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. Third, V1 receives neuromodulatory projections from subcortical structures. A feedback loop that is based on V1 and includes any neuromodulatory cell group would involve subloops with many other areas, such as the frontal cortex. Arguably, such a complex loop verges on the definition of recurrent feedback. Because neuromodulators are increasingly regarded as factors influencing sensory and cognitive processing throughout lower cortical and associational areas [12.Jacob S.N. Nienborg H. Monoaminergic neuromodulation of sensory processing.Front. Neural Circuits. 2018; 12: 51Crossref PubMed Scopus (6) Google Scholar, 13.Chandler D.J. et al.New perspectives on catecholaminergic regulation of executive circuits: evidence for independent modulation of prefrontal functions by midbrain dopaminergic and noradrenergic neurons.Front. Neural Circuits. 2014; 8: 53Crossref PubMed Scopus (33) Google Scholar, 14.Sarter M. et al.Phasic acetylcholine release and the volume transmission hypothesis: time to move on.Nat. Rev. Neurosci. 2009; 10: 383-390Crossref PubMed Scopus (179) Google Scholar], we include some of these projections in this review. Due to space restrictions, we focus on cholinergic projections from the basal forebrain whose role in the modulation of visual processing is becoming increasingly clear (e.g., [15.Pinto L. et al.Fast modulation of visual perception by basal forebrain cholinergic neurons.Nat. Neurosci. 2013; 16: 1857-1863Crossref PubMed Scopus (193) Google Scholar]). This does not mean that other neuromodulators such as noradrenaline and serotonin are less interesting or relevant, and we refer the readers to excellent prior reviews on the contributions of some of these pathways to visual processing [12.Jacob S.N. Nienborg H. Monoaminergic neuromodulation of sensory processing.Front. Neural Circuits. 2018; 12: 51Crossref PubMed Scopus (6) Google Scholar].Figure 2Feedback Projections to V1.Show full captionTop: Schematics of the anatomy of corticocortical, pulvinocortical, and cholinergic projections to V1; see also Box 1. Bottom: Recurrent projections from these three routes target specific cortical layers in V1 of primates and rodents. The relative sizes of the cortical layers are based on [81.Ji W. et al.Modularity in the organization of mouse primary visual cortex.Neuron. 2015; 87: 632-643Abstract Full Text Full Text PDF PubMed Google Scholar, 82.Balaram P. Kaas J.H. Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity.Front. Neuroanat. 2014; 8: 81Crossref PubMed Scopus (17) Google Scholar].View Large Image Figure ViewerDownload Hi-res image Download (PPT)Box 1Feedback PathwaysCorticocortical feedback projections can target V1 from frontal, temporal, or parietal cortical areas; further, they can target V1 either directly or via several steps throughout the cortical hierarchy. In primates, short-range projections from V2 target mainly layers 1, 2, and 5 and only sporadically layer 3 [83.Rockland K.S. Virga A. Terminal arbors of individual "feedback" axons projecting from area V2 to V1 in the macaque monkey: a study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin.J. Comp. Neurol. 1989; 285: 54-72Crossref PubMed Google Scholar, 84.Anderson J.C. Martin K.A.C. the synaptic connections between cortical areas V1 and V2 in macaque monkey.J. Neurosci. 2009; 29: 11283-11293Crossref PubMed Scopus (54) Google Scholar]. In mice, however, projections from secondary visual cortices target layer 1 strongly and layers 5 and 6 moderately, but layers 2–4 weakly [5.D'Souza R.D. et al.Recruitment of inhibition and excitation across mouse visual cortex depends on the hierarchy of interconnecting areas.eLife. 2016; 5e19332Crossref PubMed Scopus (12) Google Scholar]. The axonal projections to layer 1 of V1 are arranged retinotopically, overlapping with the receptive fields of V1 neurons [23.Marques T. et al.The functional organization of cortical feedback inputs to primary visual cortex.Nat. Neurosci. 2018; 21: 757-764Crossref PubMed Scopus (3) Google Scholar]. Long-range projections from the cingulate cortex to V1 mainly target layers 1 and 6 in mice [7.Zhang S. et al.Long-range and local circuits for top-down modulation of visual cortex processing.Science. 2014; 345: 660-665Crossref PubMed Scopus (202) Google Scholar], but long-range projections in primates (e.g., from the parietal cortex) have been reported to be very sparse [85.Borra E. Rockland K.S. Projections to early visual areas V1 and V2 in the calcarine fissure from parietal association areas in the macaque.Front. Neuroanat. 2011; 5: 35Crossref PubMed Scopus (25) Google Scholar].The thalamus sends feedforward projections to V1 through the LGN but also sends pulvinocortical feedback relaying information from higher cortical areas (and other brain regions; e.g., superior colliculus, basal ganglia, amygdala) to V1 [86.Doty R.W. Nongeniculate afferents to striate cortex in macaques.J. Comp. Neurol. 1983; 218: 159-173Crossref PubMed Google Scholar]. These thalamic feedback projections arise from the pulvinar in primates or the LP in rodents [9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar]. In primates, the pulvinar projects mainly to layer 1 of V1 [8.Shipp S. The functional logic of cortico–pulvinar connections.Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2003; 358: 1605-1624Crossref PubMed Scopus (0) Google Scholar]. In mice, the LP projects mostly to layer 1 but also to deep layers [9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar]. These projections show a retinotopic distribution [9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar].Most cholinergic projections from the basal forebrain collateralize and target multiple areas but can be selective between sensory cortices (e.g., targeting the auditory but not the somatosensory cortex) [87.Li X. et al.Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 415-420Crossref PubMed Scopus (0) Google Scholar, 88.Chaves-Coira I. et al.Modulation of specific sensory cortical areas by segregated basal forebrain cholinergic neurons demonstrated by neuronal tracing and optogenetic stimulation in mice.Front. Neural Circuits. 2016; 10: 28Crossref PubMed Scopus (8) Google Scholar]. Cholinergic innervation is found across all layers in V1 but is most dense in layers 1, 4, and 6 in macaques [89.Hedreen J.C. et al.Acetylcholinesterase–immunoreactive axonal network in monkey visual cortex.J. Comp. Neurol. 1984; 226: 246-254Crossref PubMed Scopus (29) Google Scholar]. In mice, cholinergic axons from the basal forebrain to V1 can be found across all layers but are most dense in layers 2/3 [87.Li X. et al.Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 415-420Crossref PubMed Scopus (0) Google Scholar]. In deep layers, these cholinergic terminals contact only inhibitory, and not excitatory, neurons through direct synaptic contacts [90.Lean G.A. et al.Cell type specific tracing of the subcortical input to primary visual cortex from the basal forebrain.J. Comp. Neurol. 2019; 527: 589-599Crossref PubMed Scopus (1) Google Scholar], but these results need to be validated for other layers. Besides such fast synaptic communication, volume transmission may be a common mechanism in cholinergic communication. Cholinergic receptors can be divided into muscarinic and nicotinic groups, which have differing prevalence across cortical layers and can be found on inhibitory as well as excitatory neurons. Thus, basal forebrain projections can engage a diversity of mechanisms, which is a theme outside the scope of this review and for which we refer to other reviews (e.g., [91.Krueger J. Disney A.A. Structure and function of dual-source cholinergic modulation in early vision.J. Comp. Neurol. 2019; 527: 738-750Crossref PubMed Scopus (0) Google Scholar]). Top: Schematics of the anatomy of corticocortical, pulvinocortical, and cholinergic projections to V1; see also Box 1. Bottom: Recurrent projections from these three routes target specific cortical layers in V1 of primates and rodents. The relative sizes of the cortical layers are based on [81.Ji W. et al.Modularity in the organization of mouse primary visual cortex.Neuron. 2015; 87: 632-643Abstract Full Text Full Text PDF PubMed Google Scholar, 82.Balaram P. Kaas J.H. Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity.Front. Neuroanat. 2014; 8: 81Crossref PubMed Scopus (17) Google Scholar]. Corticocortical feedback projections can target V1 from frontal, temporal, or parietal cortical areas; further, they can target V1 either directly or via several steps throughout the cortical hierarchy. In primates, short-range projections from V2 target mainly layers 1, 2, and 5 and only sporadically layer 3 [83.Rockland K.S. Virga A. Terminal arbors of individual "feedback" axons projecting from area V2 to V1 in the macaque monkey: a study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin.J. Comp. Neurol. 1989; 285: 54-72Crossref PubMed Google Scholar, 84.Anderson J.C. Martin K.A.C. the synaptic connections between cortical areas V1 and V2 in macaque monkey.J. Neurosci. 2009; 29: 11283-11293Crossref PubMed Scopus (54) Google Scholar]. In mice, however, projections from secondary visual cortices target layer 1 strongly and layers 5 and 6 moderately, but layers 2–4 weakly [5.D'Souza R.D. et al.Recruitment of inhibition and excitation across mouse visual cortex depends on the hierarchy of interconnecting areas.eLife. 2016; 5e19332Crossref PubMed Scopus (12) Google Scholar]. The axonal projections to layer 1 of V1 are arranged retinotopically, overlapping with the receptive fields of V1 neurons [23.Marques T. et al.The functional organization of cortical feedback inputs to primary visual cortex.Nat. Neurosci. 2018; 21: 757-764Crossref PubMed Scopus (3) Google Scholar]. Long-range projections from the cingulate cortex to V1 mainly target layers 1 and 6 in mice [7.Zhang S. et al.Long-range and local circuits for top-down modulation of visual cortex processing.Science. 2014; 345: 660-665Crossref PubMed Scopus (202) Google Scholar], but long-range projections in primates (e.g., from the parietal cortex) have been reported to be very sparse [85.Borra E. Rockland K.S. Projections to early visual areas V1 and V2 in the calcarine fissure from parietal association areas in the macaque.Front. Neuroanat. 2011; 5: 35Crossref PubMed Scopus (25) Google Scholar]. The thalamus sends feedforward projections to V1 through the LGN but also sends pulvinocortical feedback relaying information from higher cortical areas (and other brain regions; e.g., superior colliculus, basal ganglia, amygdala) to V1 [86.Doty R.W. Nongeniculate afferents to striate cortex in macaques.J. Comp. Neurol. 1983; 218: 159-173Crossref PubMed Google Scholar]. These thalamic feedback projections arise from the pulvinar in primates or the LP in rodents [9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar]. In primates, the pulvinar projects mainly to layer 1 of V1 [8.Shipp S. The functional logic of cortico–pulvinar connections.Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2003; 358: 1605-1624Crossref PubMed Scopus (0) Google Scholar]. In mice, the LP projects mostly to layer 1 but also to deep layers [9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar]. These projections show a retinotopic distribution [9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar]. Most cholinergic projections from the basal forebrain collateralize and target multiple areas but can be selective between sensory cortices (e.g., targeting the auditory but not the somatosensory cortex) [87.Li X. et al.Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 415-420Crossref PubMed Scopus (0) Google Scholar, 88.Chaves-Coira I. et al.Modulation of specific sensory cortical areas by segregated basal forebrain cholinergic neurons demonstrated by neuronal tracing and optogenetic stimulation in mice.Front. Neural Circuits. 2016; 10: 28Crossref PubMed Scopus (8) Google Scholar]. Cholinergic innervation is found across all layers in V1 but is most dense in layers 1, 4, and 6 in macaques [89.Hedreen J.C. et al.Acetylcholinesterase–immunoreactive axonal network in monkey visual cortex.J. Comp. Neurol. 1984; 226: 246-254Crossref PubMed Scopus (29) Google Scholar]. In mice, cholinergic axons from the basal forebrain to V1 can be found across all layers but are most dense in layers 2/3 [87.Li X. et al.Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 415-420Crossref PubMed Scopus (0) Google Scholar]. In deep layers, these cholinergic terminals contact only inhibitory, and not excitatory, neurons through direct synaptic contacts [90.Lean G.A. et al.Cell type specific tracing of the subcortical input to primary visual cortex from the basal forebrain.J. Comp. Neurol. 2019; 527: 589-599Crossref PubMed Scopus (1) Google Scholar], but these results need to be validated for other layers. Besides such fast synaptic communication, volume transmission may be a common mechanism in cholinergic communication. Cholinergic receptors can be divided into muscarinic and nicotinic groups, which have differing prevalence across cortical layers and can be found on inhibitory as well as excitatory neurons. Thus, basal forebrain projections can engage a diversity of mechanisms, which is a theme outside the scope of this review and for which we refer to other reviews (e.g., [91.Krueger J. Disney A.A. Structure and function of dual-source cholinergic modulation in early vision.J. Comp. Neurol. 2019; 527: 738-750Crossref PubMed Scopus (0) Google Scholar]). What functions does RP serve and through which anatomical pathways are these achieved? We highlight three main functions that have been proposed: (i) contextual modulation of stimulus processing; (ii) feedback of high-level information; and (iii) PP (Figure 1). We discuss the evidence for their dependence on RP (Table 1) and review specific criteria that need to be met for each proposed function to be mediated by recurrent feedback. Many studies have focused on stimulus-context and high-level feedback to V1 and their outcomes deliver a framework in which we discuss how RP may enable PP. Finally, we explore to what extent the three proposed functions can be integrated under an overarching functional interpretation and we discuss possible connections between RP and (conscious) perception.Table 1Empirical Findings Related to the Three Types of Feedback Projection and the Three Functions of RP that Are Discussed in this ReviewaKey: (+), evidence in favor of a match between the specified type of RP (row) and a function (column); (−), evidence against this combination.Stimulus contextHigh-level informationPPCorticocortical(+) Optogenetic silencing of V2 projections to V1 reduces stimulus-context modulation in primates 19.Nurminen L. et al.Top-down feedback controls spatial summation and response amplitude in primate visual cortex.Nat. Commun. 2018; 9: 2281Crossref PubMed Scopus (0) Google Scholar(+) In mice, projections from LM to V1 represent visual information exceeding V1 receptive fields and many projections are orientation and direction specific 23.Marques T. et al.The functional organization of cortical feedback inputs to primary visual cortex.Nat. Neurosci. 2018; 21: 757-764Crossref PubMed Scopus (3) Google Scholar(+) Laminar profile of attentional modulation in primate V1 matches a corticocortical projection profile 37.van Kerkoerle T. et al.Layer-specificity in the effects of attention and working memory on activity in primary visual cortex.Nat. Commun. 2017; 8: 13804Crossref PubMed Scopus (35) Google Scholar(+) In mice, A2b/M2 projections convey motor information to V1 52.Leinweber M. et al.A sensorimotor circuit in mouse cortex for visual flow predictions.Neuron. 2017; 95 (1420–1432.e5)Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, which is crucial to elicit prediction errors in V1 52.Leinweber M. et al.A sensorimotor circuit in mouse cortex for visual flow predictions.Neuron. 2017; 95 (1420–1432.e5)Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar, 53.Attinger A. et al.Visuomotor coupling shapes the functional development of mouse visual cortex.Cell. 2017; 169 (1291–1302.e14)Abstract Full Text Full Text PDF PubMed Scopus (19) Google Scholar(+) In mice, LM feedback to V1 extends around retinotopically matched locations; this extension is more prominent in a direction orthogonal to the LM neuron's preferred orientations; this suggests that LM neurons suppress predictive representations in V1 23.Marques T. et al.The functional organization of cortical feedback inputs to primary visual cortex.Nat. Neurosci. 2018; 21: 757-764Crossref PubMed Scopus (3) Google ScholarPulvinocortical(+/−) In mice, receptive field size and retinotopic overlap of pulvinocortical projections to V1 suggest a role during stimulus-context processing, but low orientation selectivity limits the extent of stimulus-context modulation that may occur 9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google Scholar(+) Pulvinar can be modulated by top-down attention and pharmacological silencing of this structure interferes with monkey performance in an attention task 38.Petersen S.E. et al.Contributions of the pulvinar to visual spatial attention.Neuropsychologia. 1987; 25: 97-105Crossref PubMed Scopus (231) Google Scholar; it remains unclear, however, whether this can be attributed to pulvinar-to-V1 connections(+) In mice, pulvinocortical projections convey mismatches between self-induced running speed and observed optic flow 9.Roth M.M. et al.Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex.Nat. Neurosci. 2016; 19: 299-307Crossref PubMed Scopus (0) Google ScholarCholinergic(−) The time for basal forebrain neurons to respond to stimuli (in monkeys) 28.Masuda R. et al.Neuronal responses at the sight of objects in monkey basal forebrain subregions during operant visual tasks.Neurobiol. Learn. Mem. 1997; 67: 181-196Crossref PubMed Scopus (0) Google Scholar and elicit modulation in V1 (in mice) 15.Pinto L. et al.Fast modulation of visual perception by basal forebrain cholinergic neurons.Nat. Neurosci. 2013; 16: 1857-1863Crossref PubMed Scopus (193) Google Scholar is too slow to contribute transiently to fast stimulus-context effects(+) In humans, ACh reduces spatial spread of BOLD activity in V1 25.Silver M.A. et al.Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex.Neuron. 2008; 60: 904-914Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar as well as perceptual surround suppression effects26.Kosovicheva A.A. et al.Cholinergic enhancement reduces orientation-specific surround suppression but not visual crowding.Front. Behav. Neurosci. 2012; 6: 61Crossref PubMed Scopus (9) Google Scholar(+) Iontophoretically applied ACh reduces spatial summation in primate V1 27.Roberts M.J. et al.Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex.J. Neurophysiol. 2005; 93: 2062-2072Crossref PubMed Scopus (82) Google Scholar(+) Blocking muscarinic ACh receptors reduces attentional effects in primate V1 33.Herrero J.L. et al.Acetylcholine contributes through muscarinic receptors to attentional modulation in V1.Nature. 2008; 454: 1110-1114Crossref PubMed Scopus (260) Google Scholar(+) Using neural mass models of laminar activity, it was shown that cholinergic input enhances the activity of superficial pyramidal neurons, which might code the precision of prediction errors in PP 80.Pinotsis D.A. et al.Linking canonical microcircuits and neuronal activity: dynamic causal modelling of laminar recordings.Neuroimage. 2017; 146: 355-366Crossref PubMed Scopus (3) Google Scholar(−) The latency of basal forebrain neurons in responding to stimuli (in monkeys) 28.Masuda R. et al.Neuronal responses at the sight of objects in monkey basal forebrain subregions during operant visual tasks.Neurobiol. Learn. Mem. 1997; 67: 181-196Crossref PubMed Scopus (0) Google Scholar and eliciting modulation in V1 (in mice) 15.Pinto L. et al.Fast modulation of visual perception by basal forebrain cholinergic neurons.Nat. Neurosci. 2013; 16: 1857-1863Crossref PubMed Scopus (193) Google Scholar may be too long to contribute to PPa Key: (+), evidence in favor of a match between the specified type of RP (row) and a function (column); (−), evidence against this combination. Open table in a new tab Feedback from higher cortical areas reports to the primary sensory areas a wealth of sensory information in which feedforward input is embedded. We illustrate this principle with two examples. A basic form of modulation by the sensory context around a specific visual stimulus is size tuning or surround suppression and the strongly related effect of end stopping. Responses of a V1 neuron to a small visual stimulus that matches the neuron's classical receptive field decrease when stimulus size is extended to cover the extrareceptive field, a phenomenon referred to as surround suppression [16.Knierim J.J. van Essen D.C. Neuronal responses to static texture patterns in area V1 of the alert macaque monkey.J. Neurophysiol. 1992; 67: 961-980Crossref PubMed Google Scholar, 17.Vaiceliunaite A. et al.Spatial integration in mouse primary visual cortex.J. Neurophysiol. 2013; 110: 964-972Crossref PubMed Scopus (41) Google Scholar]. Thus, a V1 neuron is tuned to a preferred stimulus size, which is large enough to cover most of