Where bottom-up meets top-down: neuronal interactions during perception and imagery.

Functional magnetic resonance imaging (fMRI) studies have identified category-selective regions in ventral occipito-temporal cortex that respond preferentially to faces and other objects. The extent to which these patterns of activation are modulated by bottom-up or top-down mechanisms is currently unknown. We combined fMRI and dynamic causal modelling to investigate neuronal interactions between occipito-temporal, parietal and frontal regions, during visual perception and visual imagery of faces, houses and chairs. Our results indicate that, during visual perception, category-selective patterns of activation in extrastriate cortex are mediated by content-sensitive forward connections from early visual areas. In contrast, during visual imagery, category-selective activation is mediated by content-sensitive backward connections from prefrontal cortex. Additionally, we report content-unrelated connectivity between parietal cortex and the category-selective regions, during both perception and imagery. Thus, our investigation revealed that neuronal interactions between occipito-temporal, parietal and frontal regions are task- and stimulus-dependent. Sensory representations of faces and objects are mediated by bottom-up mechanisms arising in early visual areas and top-down mechanisms arising in prefrontal cortex, during perception and imagery respectively. Additionally non-selective, top-down processes, originating in superior parietal areas, contribute to the generation of mental images, regardless of their content, and their maintenance in the 'mind's eye'.

[1]  J M Fuster,et al.  Visual short-term memory deficit from hypothermia of frontal cortex. , 1974, Brain research.

[2]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[3]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[4]  A. Damasio Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition , 1989, Cognition.

[5]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[6]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[7]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[8]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

[9]  S. Petersen,et al.  Functional Anatomic Studies of Memory Retrieval for Auditory Words and Visual Pictures , 1996, The Journal of Neuroscience.

[10]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[11]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[12]  J. Fuster Network memory , 1997, Trends in Neurosciences.

[13]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[14]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[15]  M. Denis,et al.  Reopening the Mental Imagery Debate: Lessons from Functional Anatomy , 1998, NeuroImage.

[16]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[17]  M. D’Esposito,et al.  An Area within Human Ventral Cortex Sensitive to “Building” Stimuli Evidence and Implications , 1998, Neuron.

[18]  D. Perani,et al.  The Effects of Semantic Category and Knowledge Type on Lexical-Semantic Access: A PET Study , 1998, NeuroImage.

[19]  Amanda Parker,et al.  The von Restorff Effect in Visual Object Recognition Memory in Humans and Monkeys: The Role of Frontal/Perirhinal Interaction , 1998, Journal of Cognitive Neuroscience.

[20]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[21]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[22]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[23]  M. Farah,et al.  A neural basis for category and modality specificity of semantic knowledge , 1999, Neuropsychologia.

[24]  Leslie G. Ungerleider,et al.  Distributed representation of objects in the human ventral visual pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[26]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[27]  Leslie G. Ungerleider,et al.  The Effect of Face Inversion on Activity in Human Neural Systems for Face and Object Perception , 1999, Neuron.

[28]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[29]  Leslie G. Ungerleider,et al.  The Representation of Objects in the Human Occipital and Temporal Cortex , 2000, Journal of Cognitive Neuroscience.

[30]  Leslie G. Ungerleider,et al.  Distributed Neural Systems for the Generation of Visual Images , 2000, Neuron.

[31]  N. Kanwisher,et al.  Mental Imagery of Faces and Places Activates Corresponding Stimulus-Specific Brain Regions , 2000, Journal of Cognitive Neuroscience.

[32]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[33]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[34]  S. Kosslyn,et al.  Functional Anatomy of High-Resolution Visual Mental Imagery , 2000, Journal of Cognitive Neuroscience.

[35]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[36]  Karl J. Friston,et al.  Nonlinear Coupling between Evoked rCBF and BOLD Signals: A Simulation Study of Hemodynamic Responses , 2001, NeuroImage.

[37]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[38]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[39]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[40]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[41]  Karl J. Friston,et al.  Dynamic representations and generative models of brain function , 2001, Brain Research Bulletin.

[42]  Leslie G. Ungerleider,et al.  Visual Imagery of Famous Faces: Effects of Memory and Attention Revealed by fMRI , 2002, NeuroImage.

[43]  Karl J. Friston,et al.  Anatomic Constraints on Cognitive Theories of Category Specificity , 2002, NeuroImage.

[44]  M. D’Esposito,et al.  Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory , 2003, Journal of Cognitive Neuroscience.

[45]  S. Kosslyn,et al.  When is early visual cortex activated during visual mental imagery? , 2003, Psychological bulletin.

[46]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[47]  Karl J. Friston,et al.  A Dynamic Causal Modeling Study on Category Effects: BottomUp or TopDown Mediation? , 2003, Journal of Cognitive Neuroscience.