ArticlePDF Available

Subcortical Contributions to the Uniqueness of Human Cognition: A Commentary on Laland & Seed (2021)

Biolinguistics 15: 12–21, 2021
Editor: Patrick C. Trettenbrein, Max Planck Institute for Human Cognitive & Brain Sciences, Germany
Received: 1 July 2021
Accepted: 24 August 2021 CC BY 4.0 License
Published: 6 September 2021 ISSN 14503417 © 2021 The authors
Subcortical Contributions
to the Uniqueness of Human Cognition:
A Commentary on Laland & Seed (2021)
Edward Ruoyang Shi1 & Elizabeth Qing Zhang2,3,4,*
1 Department of Catalan Philology and General Linguistics, University of Barcelona, Spain
2 Department of Psychology, Sun Yat-Sen University, China
3 Center for Language Evolution Studies, Nicolaus Copernicus University, Toruń, Poland
4 University Center of Excellence IMSErt Interacting Minds, Societies, Environments,
Nicolaus Copernicus University, Toruń, Poland
* Corresponding author:
1. Introduction
Laland and Seed (2021) address the issue of the evolution of human unique cog-
nition. Having reviewed comparative evidence on five candidate traitsmental
time travel, tool use, problem solving, social cognition, and communicationthe
authors conclude that no single trait could explain human superior cognition, and
humans are probably cross-domain/modality/modular thinkers leading to a
high-level intelligence which underlies human cognitive uniqueness. Such a com-
prehensively theoretical review attracts multidisciplinary readers, and the at-
tempt to answer the question of whether human cognition is unique or not is
highly significant in cognitive science. However, although the target paper pro-
vides numerous comparative data, we think that the continuous view of human
cognition is not novel.
The solution the authors offer seems to be devoid of explanatory power. We
agree that in general there is a continuum between nonhuman animal and human
cognition, and it is not surprising that human cognition is superior because infor-
mation from different modules interact. However, the authors fail to explain how
different cognitive abilities interact and why there is still a gap between human
language and animal communication systems. Take mental time travel as an ex-
ample, various animals have been shown to have limited ability to recall the past
Subcortical Contributions to the Uniqueness of Human Cognition
and predict the future (Clayton & Dickinson 2010). However, the creative use of
language enables humans to escape from current situations and produce mean-
ingful utterances that refer to things and situations outside of the here and now.
This is referred to as displacement (Hockett 1960, Bickerton 2009). It is worth not-
ing that such displacement that we focus on in this paper is distinct from that
repeatedly mentioned in the literature of generative grammar, where displace-
ment is a property of linearized syntactic structure where phrases are interpreted
in one place but pronounced in another.
We suggest that in order to achieve displacement, information from differ-
ent cognitive domains needed to be encoded into lexical items. The combination
of lexical items via syntax allows the generation of an in principle infinite number
of different syntactic structures. Syntactic operations are assumed to be domain
general, in the sense that they not only produce lexical items and sentences
(Boeckx 2014) in the language domain but also extend to other domains like music
(Shi & Zhang 2020) and movements (Pulvermüller 2014). In this commentary, we
would like to focus on displacement, and suggest that domain general syntax
serves as the underlying mechanism which enhances the combination of infor-
mation from different cognitive domains. The importance of language in human
unique cognition has been highlighted in the existing literature (e.g., Darwin 1871,
Spelke 2009, Berwick & Chomsky 2016).
From a neurocognitive perspective, we would like to further argue that syn-
tax beyond the language domain supported by the hippocampus and basal gan-
glia could play a key role. Moreover, we suggest that the interaction between
these two subcortical structures in humans gives rise to the creative use of lan-
guage that makes displacement possible which in turn lays the foundation for the
uniqueness of human cognition. We are fully aware that neuroimaging and lesion
studies point to the conclusion that syntactic operations are mainly supported by
cortical areas and cortico-cortical connections (e.g., Friederici 2011). Nevertheless,
subcortical regions have also been shown to be involved in syntactic operations
(see Shi & Zhang 2020 for a review).
From an evolutionary perspective, subcortex is conserved across species,
while neocortex is specific to mammals. Although it has been shown that neocor-
tex is important for the evolution of high-level cognition, studies on birds who
lack neocortices show that they exhibit high intelligence, like crows’ tool use
(Hunt 1996) and parrots’ vocal imitation (Chakraborty et al. 2015), suggesting an
important role of subcortex in cognition. On the other hand, if domain-general
functions of the subcortical regions lay the foundation for domain-general syntax,
it could be the case that in evolution cortical areas coordinate with subcortical
ones to achieve a better efficiency of information transformation (Shi & Zhang
2. Displacement, Other Cognitive Abilities, and a Domain-General Syntactic
Displacement is fulfilled through linguistic tools. For example, in the sentence I
played football yesterday, it is clear that both the lexical item yesterday and the syn-
tactic past tense -ed refer to an event that happened in the past. Both lexical items
Shi & Zhang
and syntax are evolutionary novelties (Bickerton 2009). Syntax not only produces
words but also puts words together into infinite combinations of phrases, clauses,
and sentences which in turn are used to express our thought. As the carrier of
displacement that makes mental time travel possible, syntax not only serves as
the engine hub for lexical items and hierarchically structured sentences in the do-
main of language but can also be extended to other domains and cognitive abili-
ties listed in Laland and Seed (2021). For example, syntactic operations have been
suggested to be analogous to tool making and use (e.g., Stout & Chaminade 2012).
Neuroimaging studies also suggest that syntactic operations and tool-making
could share the same set of neural circuits (Hecht et al. 2014; Putt et al. 2017).
Besides, language has been assumed to play an essential role in problem
solving (Baldo et al. 2005). Problem solving requires multi-facet abilities. For in-
stance, inferential reasoning, as Völter and Cho (2017) noted, usually needs the
transformations of mental representations to make predictions and the combina-
tion of spatiotemporally separate events. Hence, inferential reasoning is also
closely linked to displacement, which enables humans to predict future events at
the dimensions of both space and time.
In addition, as Laland and Seed state, language and language-related activ-
ities such as teaching play a crucial role in complex social cognition of humans.
Social cooperation is closely related to displacement. For example, in the case of
megafauna scavenging of ancient humans, when detecting a dead deinotherium,
in order to persuade other members in the group to cooperate, the members must
exchange information of where and when they found it, since only by themselves
they cannot exploit it. This kind of high-end scavenging could have distinguished
human ancestors from bone-crunching garhi and habilis.
Furthermore, Laland and Seed treat communication flexibility as the most
obvious divide between humans and other animals. They highlight the syntactic
properties “unbounded merge” (Chomsky 1995) and “recursion” (Hauser, Chom-
sky, & Fitch 2002) that underlie the creation of an infinite number of structures
and the creativity use of language which in turn allows us to cope with different
situations when we need to communicate with others. Hence, the syntactic oper-
ation serves as the prerequisite of human flexible communication.
Collectively, it seems that all five candidate traits reviewed by Laland and
Seed are related to syntactic operations. This implicates that the domain-general
thinking the authors assume could be realized with the advent of domain-general
syntactic operation. We will focus on how the domain-general syntactic operation
is supported by the subcortical regions in the following section.
3. Evidence from a Neurocognitive Perspective
At the brain level, high-level cognition could be derived from improved neural
connectivity, diversification of cell types and general cortical enlargement in evo-
lution (Striedter 2005). However, we would like to focus on how two subcortical
regions, the basal ganglia and hippocampus, and their connectivity could have
contributed to human unique cognition in the present commentary. Both areas
exhibit domain-general cognitive functions. The basal ganglia have been assumed
to be involved in motor planning and control (Wise et al. 1996), context-dependent
Subcortical Contributions to the Uniqueness of Human Cognition
rule-based selection (Peigneux et al. 2000), and sequence learning (Chan 2007).
The hippocampus serves as the hub for the interaction between semantic memory
and episodic memory (Takashima et al. 2014). Moreover, the hippocampus is not
only related to the storage of information from different cognitive domains (Tsao
et al. 2018), but is also involved in the process of relational binding which is de-
fined as
rapidly, continuously, and obligatorily form associations among dis-
parate elements across space and time, and further to enable the com-
parison of internal representations with current perceptual input.
(Olsen et al. 2012)
Both areas are also implicated in language processing. It has been estab-
lished that the cortical centered view of language network is insufficient to cover
the updated data (Kensinger et al. 2001, Teichmann et al. 2015, Copland & Angwin
2019). For example, patients with impaired basal ganglia will have symptoms sim-
ilar to non-fluent aphasia (Lieberman 2006). Further, if basal ganglia are affected
along with cortical impairment, aphasic patients’ probability to recover is lower
(Crosson et al. 2005, Shi & Zhang 2020). Hence, the contributions of subcortical
structures to language processing have received attention in cognitive and neuro-
logical research (see Shi & Zhang 2021 for a review). For example, the basal gan-
glia have been established to be related to syntactic processing of language (Kotz
et al. 2003, Friederici & Kotz 2003, Progovac et al. 2018). Further, Boeckx, Mar-
tinez-Alvarez, and Leivada (2014) proposed that the basal ganglia are involved in
the syntactic process of ‘Linearization’, the operation transferring hierarchical
syntactic structures into temporal sequences. Shi and Zhang (2020) also provide
more evidence for the functions of the basal ganglia in syntactic processing from
a clinical perspective.
The hippocampus is involved in the process of lexicalization (Takashima et
al. 2014) and lexical retrieval (Hamamé et al. 2014). Studies of developmental am-
nesia have shown that patients with atrophy of the hippocampus show difficulties
of acquiring new semantic memory (Duff et al. 2020). Recent studies have also
revealed that the hippocampus is involved in online syntactic processing (Piai et
al. 2016). Further evidence suggests that the hippocampus seems to be the inter-
face between language and memory (Shi & Zhang 2021). These functions imply
that being the possible basis for displacement as well as lexical and syntactic op-
erations, the hippocampus could play a crucial role when different cognitive abil-
ities interact.
Since both the hippocampus and basal ganglia are highly conserved brain
regions, some of their functions linked to displacement have also been found in
nonhuman animals, but very limited when compared with humans (Shi & Zhang
2021). Shi and Zhang (2021) suggest that the reason why humans have superior
displacement abilities can be partly due to the better coordination between the
hippocampus and basal ganglia.
Furthermore, the functions of the hippocampus and basal ganglia are both
domain-general, and the coordination between these two subcortical structures
has been observed in learning and memory systems. For example, the hippocam-
pus and the striatum (a subregion of the basal ganglia) were reported to be jointly
Shi & Zhang
involved in episodic memory encoding (Sadeh et al. 2011). Increased functional
connectivity between the hippocampus and striatum was also found in learning
temporal associations (van de Ven et al. 2020). Their interactions also contribute
to arbitrary associative learning (Mattfeld & Stark 2015). Moreover, the hippocam-
pal-striatal interaction is evident in spatial navigation (Goodroe, Starnes, & Brown
2018). It has also been reported that the hippocampus and striatum both play cru-
cial roles in decision-making (Johnson, van der Meer, & Redish 2007). The inter-
actions between the nucleus accumbens (a subregion of the striatum) and hippo-
campus in rats were shown to be involved in decision-making about time trade-
off (Abela, Duan & Chudasama 2015). In the domain of language, Ullman’s (2004)
declarative/procedural model posits that declarative and procedural memory,
supported by the hippocampus and basal ganglia respectively, interact with each
other in first and second language learning.
Genetic studies also provide supporting evidence. Foxp2 was discovered as
a gene affecting the coordination of speech production, together with problems in
language production and comprehension in a family with fifteen relatives pre-
senting verbal dyspraxia (the KE family; Lai et al. 2001). Two amino acid changes
were detected in exon 7 of human FOXP2 when compared with the chimpanzee
protein (Enard et al. 2002), suggesting that these two substitutions could have
played a crucial role in human evolution. Such a humanized FOXP2 inserted in
mice enhances the information transformation between procedural and declara-
tive memory (Schreiweis et al. 2014), suggesting that the basal ganglia-hippocam-
pal coordination could lead to better interaction among information from differ-
ent cognitive domains, since both brain structures are involved in multiple cogni-
tive domains. However, subsequent studies on FOXP2 revealed that the two mu-
tations found in humans is shared with Neanderthals, thus the uniqueness of the
human version FOXP2 become controversial (Fisher 2019). Nonetheless, it is less
controversial that humans are the only species acquiring language and FOXP2 is
in some way contributed to the evolution of human language.
By and large, since both subcortical regions are involved in syntactic pro-
cessing, it is reasonable to propose that it is the domain-general syntactic opera-
tion that forms the basis for domain-general interaction.
4. Conclusion
All in all, we agree with Laland and Seed (2021) that human cognitive uniqueness
arises from some combination of abilities, but we suggest that from the neurocog-
nitive perspective, the domain-general functions of the hippocampus and basal
ganglia play a key role. To be specific, we suggest that the enhanced coordination
between the hippocampus and basal ganglia possibly support domain-general
syntax which makes humans cross-modular thinking possible. In the end, we
would like to cite the following image:
Another metaphor for the cognitive effect of human language would
be the Swiss Army knife. Until language emerged, the minds of our
ancestors were full of various tools, each tailored to specific needs.
With language, all these tools were combined into a flexible all-in-one
Subcortical Contributions to the Uniqueness of Human Cognition
tool that makes available a variety of solutions (tools) whose effects
can be combined spontaneously. (Boeckx 2010: 131)
Indeed, Laland and Seed (2021) also suggest that at the higher cognitive
level, language could have enhanced the interaction between different cognitive
domains, but when language is decomposed into subcomponents at the lower
level, nothing seems to be unique to humans. This is consistent with the perspec-
tive of comparative biology that language per se is a very coarse term. In conclu-
sion, we would like to propose that it is a domain-general syntax that could serve
as the Swiss Army knife in human evolution and give rise to the uniqueness of
human cognition.
Author Contributions
Both authors jointly conceptualized and wrote the paper.
Declaration of Interest Statement
The authors declare no competing interests.
We would like to thank two anonymous reviewers for their insightful suggestions
and comments, as well as the editor for his assistance with the copyediting of our
Abela, Andrew R., Yiran Duan, & Yogita Chudasama. 2015. Hippocampal inter-
play with the nucleus accumbens is critical for decisions about time. Euro-
pean Journal of Neuroscience, 42(5). 22242233.
Baldo, Juliana V., Nina F. Dronkers, David Wilkins, Carl Ludy, Patricia Raskin, &
Jiye Kim. 2005. Is problem solving dependent on language? Brain and Lan-
guage, 92(3). 240-250.
Berwick, Robert C. & Noam Chomsky. 2016. Why Only Us: Language and Evolution.
Cambridge, MA: MIT Press.
Bickerton, Derek. 2009. Adam’s Tongue: How Humans Made Language, How Lan-
guage Made Humans. New York: Hill and Wang.
Boeckx, Cedric. 2014. Elementary Syntactic Structures: Prospects of a Feature-Free
Syntax. Cambridge: Cambridge University Press.
Boeckx, Cedric. 2010. Language in Cognition: Uncovering Mental Structures and The
Rules behind Them. Hoboken, NJ: John Wiley & Sons.
Shi & Zhang
Boeckx, Cedric, Anna Martinez-Alvarez, & Evelina Leivada. 2014. The functional
neuroanatomy of serial order in language. Journal of Neurolinguistics, 32. 1–
15. DOI: 10. 1016/j.jneuroling.2014.07.001
Chakraborty, Mukta, Solveig Walløe, Signe Nedergaard, Emma E. Fridel, Torben
Dabelsteen, Bente Pakkenberg, Mads F. Bertelsen, Gerry M. Dorrestein, Ste-
ven E. Brauth, Sarah E. Durand, & Erich D. Jarvis. 2015. Core and shell song
systems unique to the parrot brain. PLoS ONE, 10(6). 1–37.
Chan, Shiao-Hui. 2007. Linguistic Sequencing in the Cortex and Basal Ganglia. Tuc-
son, AZ: The University of Arizona PhD dissertation.
Chomsky, Noam. 1995. The Minimalist Program. Cambridge, MA: MIT Press.
Clayton, Nicola S. & Anthony Dickinson. 2010 Mental time travel: Can animals
recall the past and plan for the future? In Michael D. Breed & Janice Moore
(eds.), Encyclopedia of Animal Behavior, vol. 2, 438442. Cambridge, MA: Ac-
ademic Press.
Copland, David A. & Anthony J. Angwin. 2019. Subcortical contributions to lan-
guage. In Greig I. de Zubicaray & Niels O. Schiller (eds.), The Oxford Hand-
book of Neurolinguistics, 851876. Oxford: Oxford University Press.
Crosson, Bruce, Bruce Crosson, Anna Bacon Moore, Kaundinya Gopinath, Keith
D. White, Christina E. Wierenga, Megan E. Gaiefsky, Katherine S. Fabrizio,
Kyung K. Peck, David Soltysik, Christina Milsted, Richard W. Briggs, Tim
W. Conway, & Leslie J. Gonzalez Rothi. 2005. Role of the right and left hem-
ispheres in recovery of function during treatment of intention in aphasia.
Journal of Cognitive Neuroscience, 17(3). 392406.
Darwin, Charles. 1871. The Descent of Man and Selection in Relation to Sex. London:
J. Murray.
Duff, Melissa C., Natalie V. Covington, Caitlin Hilverman, & Neal J. Cohen. 2020.
Semantic memory and the hippocampus: Revisiting, reaffirming, and ex-
tending the reach of their critical relationship. Frontiers in Human Neurosci-
ence, 13. 471.
Enard, Wolfgang, Molly Przeworski, Simon E. Fisher, Cecilia S. L. Lai, Victor
Wiebe, Takashi Kitano, Anthony P. Monaco, & Svante Pääbo. 2002. Molec-
ular evolution of FOXP2, a gene involved in speech and language. Na-
ture, 418(6900). 869872.
Fisher, Simon E. 2019. Human genetics: The evolving story of FOXP2. Current Bi-
ology, 29(2). R65R67.
Friederici, Angela D. & Sonja A. Kotz. 2003. The brain basis of syntactic processes:
Functional imaging and lesion studies. NeuroImage, 20. S8S17.
Friederici, Angela D. 2011. The brain basis of language processing: From structure
to function. Physiological Reviews, 91(4). 13571392.
Goodroe, Sarah C., Jon Starnes, & Thackery I. Brown. 2018. The complex nature
of hippocampal-striatal interactions in spatial navigation. Frontiers in Hu-
man Neuroscience, 12. 250.
Hamamé, Carlos M., F.-Xavier Alario, Anais Llorens, Catherine Liégeois-Chauvel,
& Agnés Trébuchon-Da Fonseca. 2014. High frequency γ activity in the left
hippocampus predicts visual object naming performance. Brain and Lan-
guage. 135. 104114. DOI: 10.1016/j.bandl.2014.05.007
Hockett, Charles F. 1960. The origin of speech. Scientific American, 203(3), 8996.
Subcortical Contributions to the Uniqueness of Human Cognition
Hunt, Gavin R. 1996. Manufacture and use of hook-tools by New Caledonian
crows. Nature, 379(6562). 249251.
Hauser, Marc D., Noam Chomsky, & W. Tecumseh Fitch. 2002. The faculty of lan-
guage: What is it, who has it, and how did it evolve? Science, 298(5598).
Hecht, Erin E., Nada Khreisheh, David A.Gutman, Sean v. Taylor, JamesKilner,
A. Aldo Faisal, Bethany A. Bradley, Thierry Chaminade, & Dietrich Stout.
2014. Acquisition of paleolithic toolmaking abilities involves structural re-
modeling to inferior frontoparietal regions. Brain Structure and Function,
220(4). 23152331.
Johnson, Adam, Matthijs A. A. van der Meer, & A. David Redish. 2007. Integrating
hippocampus and striatum in decision-making. Current Opinion in Neurobi-
ology, 17(6). 692697.
Kensinger, Elizabeth A., Michael T. Ullman, & Suzanne Corkin. 2001. Bilateral
medial temporal lobe damage does not affect lexical or grammatical pro-
cessing: Evidence from amnesic patient HM. Hippocampus, 11(4). 347360.
Kotz, Sonja A., Stefan Frisch, D. Yves Von Cramon, & Angela D. Friederici. 2003.
Syntactic language processing: ERP lesion data on the role of the basal gan-
glia. Journal of the International Neuropsychological Society, 9(7). 10531060.
Lai, Cecilia S. L., Simon E. Fisher, Jane A. Hurst, Faraneh Vargha-Khadem, & An-
thony P. Monaco. 2001. A forkhead-domain gene is mutated in a severe
speech and language disorder. Nature, 413(6855). 519523.
Laland, Kevin & Amanda Seed. 2021. Understanding human cognitive unique-
ness. Annual Review of Psychology, 72. 689716.
Lieberman, Philip. 2006. Toward an Evolutionary Biology of Language. Cambridge,
MA: Harvard University Press.
Leisman, Gerry, Orit Braun-Benjamin, & Robert Melillo. 2014. Cognitive-motor
interactions of the basal ganglia in development. Frontiers in Systems Neuro-
science, 8. 16.
Mattfeld, Aaron T. & Craig E. L. Stark. 2015. Functional contributions and inter-
actions between the human hippocampus and subregions of the striatum
during arbitrary associative learning and memory. Hippocampus, 25(8). 900
Olsen, Rosanna Kathleen, Sandra N. Moses, Lily Riggs, & Jennifer D. Ryan. 2012.
The hippocampus supports multiple cognitive processes through relational
binding and comparison. Frontiers in Human Neuroscience, 6. 146.
Peigneux, Philippe, Pierre Maquet, Thierry Meulemans, Arnaud Destrebecqz, Ste-
ven Laureys, Christian Degueldre, Guy Delfiore, Joël Aerts, André Luxen,
Georges Franck, Marlies van der Linden, & Axel Cleeremans. 2000. Striatum
forever, despite sequence learning variability: A random effect analysis of
pet data. Human Brain Mapping, 10(4). 17994.
Piai, Vitória, Kristopher L. Andersona, Jack J. Lind, Callum Dewara, Josef Par-
vizie, Nina F. Dronkers, & Robert T. Knight. 2016. Direct brain recordings
reveal hippocampal rhythm underpinnings of language processing. Proceed-
ings of the National Academy of Sciences of the United States of America, 113(40).
Shi & Zhang
Progovac, Ljiljana, Natalia Rakhlin, William Angell, Ryan Liddane, Lingfei Tang,
& Noa Ofen. 2018. Neural correlates of syntax and proto-syntax: Evolution-
ary dimension. Frontiers in Psychology, 9. 2415.
Pulvermüller, Friedemann. 2014. The syntax of action. Trends in Cognitive. Science.
18. 219220.
Putt, Shelby S., Sobanawartiny Wijeakumar, Robert G. Franciscus, & John P. Spen-
cer. 2017. The functional brain networks that underlie Early Stone Age tool
manufacture. Nature Human Behaviour, 1(6). 0102.
Sadeh, Talya, et al. 2011. Cooperation between the hippocampus and the striatum
during episodic encoding. Journal of Cognitive Neuroscience, 23(7). 15971608.
Schreiweis, Christiane, Ulrich Bornschein, Eric Burguière, Cemil Kerimoglu, Sven
Schreiter, Michael Dannemann, Shubhi Goyal, Ellis Rea, Catherine A.
French, Rathi Puliyadi, Matthias Groszer, Simon E. Fisher, Roger Mundry,
Christine Winter, Wulf Hevers, Svante Pääbo, Wolfgang Enard, & Ann M.
Graybiel. 2014. Humanized Foxp2 accelerates learning by enhancing transi-
tions from declarative to procedural performance. Proceedings of the National
Academy of Sciences of the United States of America, 111(39). 1425314258.
Shi, Edward Ruoyang & Qing Zhang. 2020. A domain-general perspective on the
role of the basal ganglia in language and music: Benefits of music therapy
for the treatment of aphasia. Brain and Language, 206. 104811.
Shi, Edward Ruoyang & Qing Zhang. 2021. Displacement and evolution: A neu-
rocognitive and comparative perspective. Proceedings of the 43rd Annual
Meeting of the Cognitive Science Society Comparative CognitionAnimal
Minds, (Cogsci 2021), 43. 18791885.
Spelke, Elizabeth S. 2009. Forum. In Michael Tomasello (ed.), Why We Cooperate,
149172. Cambridge, MA: MIT Press.
Stout, Dietrich & Thierry Chaminade. 2012. Stone tools, language and the brain in
human evolution. Philosophical Transactions of the Royal Society B: Biological
Sciences, 367(1585). 7587.
Striedter, George F. 2005. Principles of Brain Evolution. Sunderland, MA: Sinauer.
Takashima, Atsuko, Iske Bakker, Janet G van Hell, Gabriele Janzen, & James M
McQueen. 2014. Richness of information about novel words influences how
episodic and semantic memory networks interact during lexicaliza-
tion. NeuroImage, 84. 265-278.
Teichmann, Marc, Charlotte Rosso, Jean-Baptiste Martini, Isabelle Bloch, Pierre
Brugieres, Hugues Duffau, Stephane Lehericy, & Anne-Catherine Bachoud-
Lévi. 2015. A cortical-subcortical syntax pathway linking Broca’s area and
the striatum. Human Brain Mapping, 36(6). 22702283.
Tsao, Alber, Jørgen Sugar, Li Lu, Cheng Wang, James J. Knierim, May-Britt Moser,
& Edvard I. Moser. 2018. Integrating time from experience in the lateral en-
torhinal cortex. Nature, 561(7721). 5762.
Ullman, Michael T. 2004. Contributions of memory circuits to language: The de-
clarative/procedural model. Cognition, 92(12). 231270.
van de Ven, Vincent, Chanju Lee, Julia Lifanov, Sarah Kochs, Henk Jansma, &
Peter De Weerd. 2020. Hippocampal-striatal functional connectivity sup-
ports processing of temporal expectations from associative memory. Hippo-
campus, 30(9). 926937.
Subcortical Contributions to the Uniqueness of Human Cognition
Völter, Christoph J. & Josep Call. 2017. Causal and inferential reasoning in ani-
mals. In Josep Call (ed.), APA Handbook of Comparative Psychology, vol. 2: Per-
ception, Learning and Cognition, 64371. Washington, DC: American Psycho-
logical Association.
Wise, Steven P., Elizabeth A. Murray, & Charles R. Gerfen. 1996. The frontal cor-
tex-basal ganglia system in primates. Critical Reviews in Neurobiology, 10.
ResearchGate has not been able to resolve any citations for this publication.
Full-text available
The hippocampus and dorsal striatum are both associated with temporal processing, but they are thought to play distinct roles. The hippocampus has been reported to contribute to storing temporal structure of events in memory, whereas the striatum contributes to temporal motor preparation and reward anticipation. Here, we asked whether the striatum cooperates with the hippocampus in processing the temporal context of memorized visual associations. In our task, participants were trained to implicitly form temporal expectations for one of two possible time intervals associated to specific cue‐target associations, and subsequently were scanned using ultra‐high‐field 7T functional magnetic resonance imaging. During scanning, learned temporal expectations could be violated when the pairs were presented at either the associated or not‐associated time intervals. When temporal expectations were met during testing trials, activity in left and right hippocampal subfields and right putamen decreased, compared to when temporal expectations were not met. Further, psycho‐physiological interactions showed that functional connectivity between left hippocampal subfields and caudate decreased when temporal expectations were not met. Our results indicate that the hippocampus and striatum cooperate to process implicit temporal expectation from mnemonic associations. Our findings provide further support for a hippocampal‐striatal network in temporal associative processing.
Full-text available
Since Tulving proposed a distinction in memory between semantic and episodic memory, considerable effort has been directed towards understanding their similar and unique features. Of particular interest has been the extent to which semantic and episodic memory have a shared dependence on the hippocampus. In contrast to the definitive evidence for the link between hippocampus and episodic memory, the role of the hippocampus in semantic memory has been a topic of considerable debate. This debate stems, in part, from highly variable reports of new semantic memory learning in amnesia ranging from profound impairment to full preservation, and various degrees of deficit and ability in between. More recently, a number of significant advances in experimental methods have occurred, alongside new provocative data on the role of the hippocampus in semantic memory, making this an ideal moment to revisit this debate, to re-evaluate data, methods, and theories, and to synthesize new findings. In line with these advances, this review has two primary goals. First, we provide a historical lens with which to reevaluate and contextualize the literature on semantic memory and the hippocampus. The second goal of this review is to provide a synthesis of new findings on the role of the hippocampus and semantic memory. With the perspective of time and this critical review, we arrive at the interpretation that the hippocampus does indeed make necessary contributions to semantic memory. We argue that semantic memory, like episodic memory, is a highly flexible, (re)constructive, relational and multimodal system, and that there is value in developing methods and materials that fully capture this depth and richness to facilitate comparisons to episodic memory. Such efforts will be critical in addressing questions regarding the cognitive and neural (inter)dependencies among forms of memory, and the role that these forms of memory play in support of cognition more broadly. Such efforts also promise to advance our understanding of how words, concepts, and meaning, as well as episodes and events, are instantiated and maintained in memory and will yield new insights into our two most quintessentially human abilities: memory and language.
Full-text available
The present fMRI study tested predictions of the evolution-of-syntax framework which analyzes certain structures as remnants (“fossils”) of a non-hierarchical (non-recursive) proto-syntactic stage in the evolution of language (Progovac, 2015, 2016). We hypothesized that processing of these structures, in comparison to more modern hierarchical structures, will show less activation in the brain regions that are part of the syntactic network, including Broca’s area (BA 44 and 45) and the basal ganglia, i.e., the network bolstered in the line of descent of humans through genetic mutations that contributed to present-day dense neuronal connectivity among these regions. Fourteen healthy native English-speaking adults viewed written stimuli consisting of: (1) full sentences (FullS; e.g., The case is closed); (2) Small Clauses (SC; e.g., Case closed); (3) Complex hierarchical compounds (e.g., joy-killer); and (4) Simple flat compounds (e.g., kill-joy). SC (compared to FullS) resulted in reduced activation in the left BA 44 and right basal ganglia. Simple (relative to complex) compounds resulted in increased activation in the inferior temporal gyrus and the fusiform gyrus (BA 37/19), areas implicated in visual and semantic processing. We discuss our findings in the context of current theories regarding the co-evolution of language and the brain.
Full-text available
The encoding of time and its binding to events are crucial for episodic memory, but how these processes are carried out in hippocampal-entorhinal circuits is unclear. Here we show in freely foraging rats that temporal information is robustly encoded across time scales from seconds to hours within the overall population state of the lateral entorhinal cortex. Similarly pronounced encoding of time was not present in the medial entorhinal cortex or in hippocampal areas CA3-CA1. When animals' experiences were constrained by behavioural tasks to become similar across repeated trials, the encoding of temporal flow across trials was reduced, whereas the encoding of time relative to the start of trials was improved. The findings suggest that populations of lateral entorhinal cortex neurons represent time inherently through the encoding of experience. This representation of episodic time may be integrated with spatial inputs from the medial entorhinal cortex in the hippocampus, allowing the hippocampus to store a unified representation of what, where and when.
Full-text available
Decades of research have established the importance of the hippocampus for episodic and spatial memory. In spatial navigation tasks, the role of the hippocampus has been classically juxtaposed with the role of the dorsal striatum, the latter of which has been characterized as a system important for implementing stimulus-response and action-outcome associations. In many neuroimaging paradigms, this has been explored through contrasting way finding and route-following behavior. The distinction between the contributions of the hippocampus and striatum to spatial navigation has been supported by extensive literature. Convergent research has also underscored the fact that these different memory systems can interact in dynamic ways and contribute to a broad range of navigational scenarios. For example, although familiar routes may often be navigable based on stimulus-response associations, hippocampal episodic memory mechanisms can also contribute to egocentric route-oriented memory, enabling recall of context-dependent sequences of landmarks or the actions to be made at decision points. Additionally, the literature has stressed the importance of subdividing the striatum into functional gradients—with more ventral and medial components being important for the behavioral expression of hippocampal-dependent spatial memories. More research is needed to reveal how networks involving these regions process and respond to dynamic changes in memory and control demands over the course of navigational events. In this Perspective article, we suggest that a critical direction for navigation research is to further characterize how hippocampal and striatal subdivisions interact in different navigational contexts.
Full-text available
After 800,000 years of making simple Oldowan tools, early humans began manufacturing Acheulian handaxes around 1.75 million years ago. This advance is hypothesized to reflect an evolutionary change in hominin cognition and language abilities. We used a neuroarchaeology approach to investigate this hypothesis, recording brain activity using functional near-infrared spectroscopy as modern human participants learned to make Oldowan and Acheulian stone tools in either a verbal or nonverbal training context. Here we show that Acheulian tool production requires the integration of visual, auditory and sensorimotor information in the middle and superior temporal cortex, the guidance of visual working memory representations in the ventral precentral gyrus, and higher-order action planning via the supplementary motor area, activating a brain network that is also involved in modern piano playing. The right analogue to Broca’s area—which has linked tool manufacture and language in prior work1,2—was only engaged during verbal training. Acheulian toolmaking, therefore, may have more evolutionary ties to playing Mozart than quoting Shakespeare.
Full-text available
Significance Language is viewed as a predominantly perisylvian function typically studied in isolation from memory. We demonstrate that the same neuronal computations used by the hippocampus for memory function also subserve online language usage. Our findings specify that the hippocampal complex contributes to language in an active fashion, relating incoming words to stored semantic knowledge, a necessary process in the generation of sentence meaning. These findings represent a major step in integrating the studies of language and memory, significantly expanding the role of hippocampal theta oscillations and adding hippocampal structures to the neural network supporting language.
FOXP2 mutations cause a speech and language disorder, raising interest in potential roles of this gene in human evolution. A new study re-evaluates genomic variation at the human FOXP2 locus but finds no evidence of recent adaptive evolution.