Supramodal numerosity selectivity of neurons in primate prefrontal and posterior parietal cortices

Nieder, Andreas

doi:10.1073/pnas.1204580109

Cited by 169 publications

(189 citation statements)

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“…Second, neuronal discharges of selective neurons proved to be relevant for the crows' correct performance; if the neurons did not properly encode their preferred numerosity, the crow was prone to make mistakes. Similar results have been reported repeatedly for numerosity-selective neurons in monkeys (10)(11)(12)(13)(14)(15)(16)(17)(18). Third, both the neuronal and the behavioral tuning functions were best described on a logarithmic number line, arguing for a nonlinearly compressed coding of numerical information.…”

Section: Discussionsupporting

confidence: 68%

“…Our behavioral and neuronal data show an impressive correspondence of neuronal mechanisms found in the avian brain with those reported earlier in the nonhuman and human primate brain: First, NCL neurons were tuned to individual preferred numerosities characteristic of a "labeled-line code," enabling an unequivocal representation of numerosity by a neuronal population. Complementary findings have been made in the monkey prefrontal and posterior parietal cortex; both in the highly trained (10)(11)(12)(13)(14)(15)(16)(17)(18) and in the numerically naïve monkey (30), numerosity is encoded by a labeled-line code. Second, neuronal discharges of selective neurons proved to be relevant for the crows' correct performance; if the neurons did not properly encode their preferred numerosity, the crow was prone to make mistakes.…”

Section: Discussionmentioning

confidence: 99%

“…The neuronal correlates of numerosity representations have only been explored in humans (7)(8)(9) and primates (10)(11)(12)(13)(14)(15)(16)(17)(18), and they have been found to reside in the prefrontal and posterior parietal neocortices. In contrast to primates, birds lack a six-layered neocortex.…”

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confidence: 99%

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Neurons selective to the number of visual items in the corvid songbird endbrain

Ditz

Nieder

2015

Proc. Natl. Acad. Sci. U.S.A.

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It is unknown whether anatomical specializations in the endbrains of different vertebrates determine the neuronal code to represent numerical quantity. Therefore, we recorded single-neuron activity from the endbrain of crows trained to judge the number of items in displays. Many neurons were tuned for numerosities irrespective of the physical appearance of the items, and their activity correlated with performance outcome. Comparison of both behavioral and neuronal representations of numerosity revealed that the data are best described by a logarithmically compressed scaling of numerical information, as postulated by the WeberFechner law. The behavioral and neuronal numerosity representations in the crow reflect surprisingly well those found in the primate association cortex. This finding suggests that distantly related vertebrates with independently developed endbrains adopted similar neuronal solutions to process quantity.single-cell recordings | crow | nidopallium caudolaterale | quantity B irds show elaborate quantification skills (1-3) that are of adaptive value in naturalistic situations like nest parasitism (4), food caching (5), or communication (6). The neuronal correlates of numerosity representations have only been explored in humans (7-9) and primates (10-18), and they have been found to reside in the prefrontal and posterior parietal neocortices. In contrast to primates, birds lack a six-layered neocortex. The birds' lineage diverged from mammals 300 Mya (19), at a time when the neocortex had not yet developed from the pallium of the endbrain. Instead, birds developed different pallial parts as dominant endbrain structures (20, 21) based on convergent evolution, with the nidopallium caudolaterale (NCL) as a highlevel association area (22-26). Where and how numerosity is encoded in vertebrates lacking a neocortex is unknown. Here, we show that neurons in the telencephalic NCL of corvid songbirds respond to numerosity and show a specific code for numerical information. ResultsCrows were trained in a delayed matching-to-sample task to match the number of (one to five) dots presented on touch-sensitive computer displays ( Fig. 1 A and B). Crows watched two displays (first sample, then test) separated by a 1-s delay. They were trained to peck at the displays on the screen if the test displays contained the same number of items as the sample. We varied the exact physical appearance of the displays by randomly placing dots in arbitrary locations, and by randomly choosing dot size.The crows performed the task proficiently (73.8 ± 0.4% and 77.5 ± 0.5% correct over all recording sessions for crow A and crow J, respectively; Fig. 1C). Average performance of both crows was significantly better than chance (50%) for all sample numerosities relative to the numerically most distant nonmatches (Binomial test, P < 0.01). Better performance for sample numerosities at the low (one) and high (five) numerosity range (Fig. 1D) are most likely due to "endeffects," because one and five items had to be discriminated only fro...

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Section: Discussionsupporting

confidence: 68%

Section: Discussionmentioning

confidence: 99%

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Neurons selective to the number of visual items in the corvid songbird endbrain

Ditz

Nieder

2015

Proc. Natl. Acad. Sci. U.S.A.

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155

187

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“…The prefrontal region at the apex of the cortical hierarchy processes social signals 35 and thus could be strategically situated to regulate communicative signals. Neurons in the PFC receive highly processed information to represent abstract categories 46,47 irrespective of sensory modality 48 . The PFC actively retrieves associative representations from long-term memory for top-down control 49 and establishes semantic associations between arbitrary items and meaningful categories 50,51 .…”

Section: Discussionmentioning

confidence: 99%

Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations

2013

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Broca's area in the ventrolateral prefrontal cortex (vlPFC) has a crucial role in human volitional speech production; damage to this area causes severe impairment of speech production. Lesions in PFC of monkeys, however, have only mild effects on spontaneous vocal behaviour. Non-human primate vocalizations are thus believed to constitute affective utterances processed by a subcortical network. Here in contrast to this assumption, we show that rhesus monkeys can control their vocalizations in a goal-directed way. During single-cell recordings in the vlPFC of monkeys trained to vocalize in response to visual cues, we find call-related neurons that specifically predict the preparation of instructed vocalizations. The activity of many call-related neurons before vocal output correlates with call parameters of instructed vocalizations. These findings suggest a cardinal role of the monkey homologue of Broca's area in vocal planning and call initiation, a putative phylogenetic precursor in non-human primates for speech control in linguistic humans.

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“…In addition, studies have shown that neurons in the PFC of numerically naive monkeys tune to a preferred numerosity [48] , independent of sensory modality [49] . These neurons may potentially subserve the neuronal mechanisms underlying WM quantity.…”

Section: Prefrontal Cortex and Wm Quantitymentioning

confidence: 99%

Prefrontal cortex and sensory cortices during working memory: quantity and quality

Bodner

Zhou

2015

Neurosci. Bull.

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The activity in sensory cortices and the prefrontal cortex (PFC) throughout the delay interval of working memory (WM) tasks refl ect two aspects of WM-quality and quantity, respectively. The delay activity in sensory cortices is fi ne-tuned to sensory information and forms the neural basis of the precision of WM storage, while the delay activity in the PFC appears to represent behavioral goals and filters out irrelevant distractions, forming the neural basis of the quantity of task-relevant information in WM. The PFC and sensory cortices interact through different frequency bands of neuronal oscillation (theta, alpha, and gamma) to fulfi ll goal-directed behaviors.Keywords: working memory; prefrontal cortex; capacity limit; memory precision; neuronal oscillations ·Review· IntroductionWorking memory (WM) refers to the cognitive processes of maintaining and storing information in the short term (usually seconds) for subsequent goal-directed action [1][2][3] . Persistent activity in both sensory cortices and association areas (especially the prefrontal cortex, PFC) throughout the delay interval of a WM task after sensory stimulus presentation (sample) are usually considered to be critical for WM maintenance, and to bridge the temporal gap between the sample and the subsequent contingent response (see reviews [4,5] ). However, with regard to WM the role of the delay activity in sensory cortices has been thought to differ from that of the PFC. The former has been thought to represent and store selective sensory information and the latter has been considered to exert attentional bias and cognitive control over the former (see reviews [6,7] ).Despite the vast storage in human long-term memory, WM has been demonstrated to have a capacity limited by the number of items [8,9] and this is strongly correlated with general cognitive ability [10,11] . Recent advances in studying visual WM have shown a precision limit of representations in WM besides the capacity limit [12][13][14][15][16] .Combined with the above findings, we propose that delay activity in the sensory cortices and PFC reflect the quality and quantity of representations in WM, respectively. Specifically, in this review, quantity refers to how many items/slots are stored in working memory, and quality refers to how precisely the features of each item/slot are represented in WM. Sensory Cortices and the Quality of Working MemoryNeurons in the PFC have been shown to respond to sensory stimuli in WM tasks [17,18] . Compared with those PFC neurons, neurons in sensory cortices appear to be more selectively tuned to stimulus features in WM tasks Neurosci Bull April 1, 2015, 31(2): 175-182 176 and consequently to maintain high-fi delity representations of stimulus information in the service of WM [19] .Some human imaging as well as neurophysiological studies in non-human primates have indicated an absence of persistent activity in early sensory regions [20][21][22][23][24] . However, other primate studies have revealed persistent modulation of neuronal activity i...

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Supramodal numerosity selectivity of neurons in primate prefrontal and posterior parietal cortices

Cited by 169 publications

References 45 publications

Neurons selective to the number of visual items in the corvid songbird endbrain

Neurons selective to the number of visual items in the corvid songbird endbrain

Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations

Prefrontal cortex and sensory cortices during working memory: quantity and quality

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