Hierarchical organization of macaque and cat cortical sensory systems explored with a novel network processor
Open accessAbstract
Neuroanatomists have described a large number of connections between the various structures of monkey and cat cortical sensory systems. Because of the complexity of the connection data, analysis is required to unravel what principles of organization they imply. To date, analysis of laminar origin and termination connection data to reveal hierarchical relationships between the cortical areas has been the most widely acknowledged approach. We programmed a network processor that searches for optimal hierarchical orderings of cortical areas given known hierarchical constraints and rules for their interpretation. For all cortical systems and all cost functions, the processor found a multitude of equally low–cost hierarchies. Laminar hierarchical constraints that are presently available in the anatomical literature were therefore insufficient to constrain a unique ordering for any of the sensory systems we analysed. Hierarchical orderings of the monkey visual system that have been widely reported, but which were derived by hand, were not among the optimal orderings. All the cortical systems we studied displayed a significant degree of hierarchical organization, and the anatomical constraints from the monkey visual and somatomotor systems were satisfied with very few constraint violations in the optimal hierarchies. The visual and somato–motor systems in that animal were therefore surprisingly strictly hierarchical. Most inconsistencies between the constraints and the hierarchical relationships in the optimal structures for the visual system were related to connections of area FST (fundus of superior temporal sulcus). W e found that the hierarchical solutions could be further improved by assuming that FSTconsists of two areas, which differ in the nature of their projections. Indeed, we found that perfect hierarchical arrangements of the primate visual system, without any violation of anatomical constraints, could be obtained under two reasonable conditions, namely the subdivision of FST into two distinct areas, whose connectivity we predict, and the abolition of at least one of the less reliable rule constraints. Our analyses showed that the future collection of the same type of laminar constraints, or the inclusion of new hierarchical constraints from thalamocortical connections, will not resolve the problem of multiple optimal hierarchical representations for the primate visual system. Further data, however, may help to specify the relative ordering of some more areas. This indeterminacy of the visual hierarchy is in part due to the reported absence of some connections between cortical areas. These absences are consistent with limited cross–talk between differentiated processing streams in the system. Hence, hierarchical representation of the visual system is affected by, and must take into account, other organizational features, such as processing streams.
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- Authors
- Hilgetag, C., O'Neill, M. A., & Young, M. P.
- Affiliations
- Newcastle University (GB)
- Mural Systems Group, Department of Psychology, University of Newcastle upon Tyne, Ridley Building, Newcastle uponTyne NE1 7RU, UK
- Corresponding author
- Hilgetag, Claus–C.
- ORCID
- Hilgetag, Claus–C.
- Venue
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2000-01-29
- Volume
- 355
- Issue
- 1393
- Pages
- 71-89
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC1692720
- OpenAlex
- W2049663217
- Cited by
- 167
- References
- 36
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 6 · 2023: 8 · 2022: 4 · 2021: 9 · 2020: 8 · 2019: 8 · 2018: 8 · 2017: 6 · 2016: 10 · 2015: 6 · 2014: 5 · 2013: 7 · 2012: 6
- FWCI
- 3.19
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- cortical hierarchy, macaque, cats, network processors, primate visual system, thalamocortical connections, cortical connectivity
- MeSH terms
- Algorithms, Animals, Cats, Computer Simulation, Biological Evolution, Limbic System, Macaca, Models, Neurological, Motor Neurons, Neurons, Afferent, Somatosensory Cortex, Visual Cortex, Visual Pathways
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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