Daniela Vallentin

Relating magnitudes: the brain's code for proportions

Whereas much is known about how we categorize and reason based on absolute quantity, data exploring ratios of quantities, as in proportions and fractions, are comparatively sparse. Until recently, it remained elusive whether these two representations of number are connected, how proportions are implemented by neurons and how language shapes this code. New data derived with complementary methods and from different model systems now shed light on the mechanisms of magnitude ratio representations. A coding scheme for proportions has emerged that is remarkably reminiscent of the representation of absolute number. These novel findings suggest a sense for ratios that grants the brain automatic access to proportions independently of language and the format of presentation.

Behavioral and Prefrontal Representation of Spatial Proportions in the Monkey

Primate brains are equipped with evolutionarily old and dedicated neural circuits so that they can grasp absolute quantities, such as the number of items or the length of a line. Absolute magnitude, however, is often not informative enough to guide decisions in conflicting social and foraging situations that require an assessment of quantity ratios. We report that rhesus monkeys can discriminate proportions (1:4, 2:4, 3:4, and 4:4) specified by bars differing in lengths and that they can do so at a precision comparable to that shown by humans; the monkeys thus demonstrate an abstract understanding of proportionality. Moreover, neurons in the lateral prefrontal cortex selectively responded to preferred proportions regardless of the exact physical appearance of the stimuli. These results support the hypothesis that nonhuman primates can judge proportions and utilize the underlying information in behaviorally relevant situations.

Excitation and Inhibition Compete to Control Spiking during Hippocampal Ripples: Intracellular Study in Behaving Mice

High-frequency ripple oscillations, observed most prominently in the hippocampal CA1 pyramidal layer, are associated with memory consolidation. The cellular and network mechanisms underlying the generation of the rhythm and the recruitment of spikes from pyramidal neurons are still poorly understood. Using intracellular, sharp electrode recordings in freely moving, drug-free mice, we observed consistent large depolarizations in CA1 pyramidal cells during sharp wave ripples, which are associated with ripple frequency fluctuation of the membrane potential (“intracellular ripple”). Despite consistent depolarization, often exceeding pre-ripple spike threshold values, current pulse-induced spikes were strongly suppressed, indicating that spiking was under the control of concurrent shunting inhibition. Ripple events were followed by a prominent afterhyperpolarization and spike suppression. Action potentials during and outside ripples were orthodromic, arguing against ectopic spike generation, which has been postulated by computational models of ripple generation. These findings indicate that dendritic excitation of pyramidal neurons during ripples is countered by shunting of the membrane and postripple silence is mediated by hyperpolarizing inhibition.

Inhibition protects acquired song segments during vocal learning in zebra finches

Fixation on learned syllables Zebra finches learn their beautiful songs by listening to other zebra finches. Vallentin et al. observed zebra finch brains as learning proceeded, only to find that inhibition of the neuronal circuits was critical to fixating on learned sequences. For song syllables that have been adequately learned, the inhibitory neurons fired coherently. Song syllables not yet learned failed to produce this flag. Thus, it is the learning process that alters the neuronal circuits. The inhibitory neuronal firing, not the age of the bird, locks in the learning. Science, this issue p. 267 Songs that birds have already learned are preserved by inhibitory neurons that block further modifications. Vocal imitation involves incorporating instructive auditory information into relevant motor circuits through processes that are poorly understood. In zebra finches, we found that exposure to a tutor’s song drives spiking activity within premotor neurons in the juvenile, whereas inhibition suppresses such responses upon learning in adulthood. We measured inhibitory currents evoked by the tutor song throughout development while simultaneously quantifying each bird’s learning trajectory. Surprisingly, we found that the maturation of synaptic inhibition onto premotor neurons is correlated with learning but not age. We used synthetic tutoring to demonstrate that inhibition is selective for specific song elements that have already been learned and not those still in refinement. Our results suggest that structured inhibition plays a crucial role during song acquisition, enabling a piece-by-piece mastery of complex tasks.

Numerical Rule Coding in the Prefrontal, Premotor, and Posterior Parietal Cortices of Macaques

Switching flexibly between behavioral goals is a hallmark of executive control and requires integration of external and internal information. We recorded single-neuron correlates of different numerical representations (sensory-, working memory-, and rule-related activity) in the dorsal premotor area (PMd), the cingulate motor areas (CMA), and the ventral intraparietal sulcus (VIP) and compared them to previous recordings in the lateral prefrontal cortex (PFC). Two monkeys were trained to encode and memorize numerosities and flexibly switch between two abstract quantitative rules based on rule cues. Almost 20% of randomly selected PFC and PMd neurons significantly represented the numerical rule in a behaviorally relevant manner, approximately twice as many as in the CMA and VIP. Rule selectivity was significantly better for PMd neurons than for PFC cells. Seemingly at the expense of rule selectivity, however, sensory- and memory-related numerosity activity was greatly diminished compared with previous delayed match-to-numerosity studies. These findings suggest the involvement of the frontal premotor areas in strategic planning such as rule following. Moreover, the results emphasize that the coding capacities of neurons in association cortical areas are far more dynamic depending on task demands than previously thought.

Representations of visual proportions in the primate posterior parietal and prefrontal cortices

The primate prefrontal (PFC) and posterior parietal cortices (PPC) have been shown to be cardinal structures in processing abstract absolute magnitudes, such as numerosity or length. The neuronal representation of quantity relations, however, remained largely elusive. Recent functional imaging studies in humans showed that blood flow changes systematically both in the PFC and the PPC as a function of relational distance between proportions. We investigated the response properties of single neurons in the lateral PFC and the inferior parietal lobule (IPL, area 7) in rhesus monkeys performing a lengths‐proportion‐discrimination task. Neurons in both areas shared many characteristics and showed peaked tuning functions with preferred proportions. However, a significantly higher percentage of neurons coding proportions was found in the PFC compared with the IPL. In agreement with human studies, our study shows that proportions are represented in the fronto‐parietal network that has already been implicated for absolute magnitude processing.

Neuronal representation of number and proportion in the primate brain

Number symbols have allowed humans to develop superior mathematical skills that are a hallmark of technologically advanced cultures. Findings in animal cognition, developmental psychology, and anthropology indicate that these numerical skills are rooted in nonlinguistic biological primitives. Recent studies in human and nonhuman primates using a broad range of methodologies provide evidence that numerical information is represented and processed by regions of the prefrontal and posterior parietal lobes, where single neurons are tuned to preferred absolute quantities. Until recently, data exploring ratios of quantities, as in proportions and fractions, were comparatively sparse. New data derived with complementary methods and from different model systems now shed light on the mechanisms of magnitude ratio representations. A coding scheme for proportions has emerged that is highly reminiscent of the representation of absolute number. The magnitude code is automatic, independent of language and the format of presentation. These findings suggest that the primate brain houses a phylogenetically old network for the representation of quantity that, during the course of human evolution, has been coopted to build our remarkable sense of number.

Neurobiologische Grundlagen der Verarbeitung von Anzahlen und Proportionen im Primatengehirn

Zusammenfassung Die Erfindung von Zahlensymbolen war ein entscheidender Schritt hin zur Entwicklung ausgeprägter mathematischer Fähigkeiten des Menschen, die ihrerseits den wissenschaftlich- technologischen Fortschritt ermöglichten. Vielfältige Studien zeigen, dass das grundlegende Verständnis von Anzahlen und Mengen nicht humanspezifisch, sondern im gesamten Tierreich verbreitet ist. Die Erforschung der neuronalen Grundlagen der numerischen Kognition hat in den letzten Jahren entscheidende Fortschritte erzielt. Bildgebende Verfahren beim Menschen und Einzelzellableitungen bei nicht-humanen Primaten konnten Regionen des Gehirns identifizieren und näher charakterisieren, die eine zentrale Rolle bei der Repräsentation von Quantitäten spielen. Es zeigte sich, dass sich im Stirn- und Scheitellappen der Großhirnrinde Neurone befinden, die auf Anzahlen und Proportionen abgestimmt sind. Quantitäten werden als analoge Größen repräsentiert; dieser Code ist automatisch, unabhängig vom Darstellungsformat und nicht an Sprache gebunden. Diese Befunde legen nahe, dass unser Sinn für Zahlen auf einem phylogenetisch alten Vorläufersystem zur Repräsentation von Quantitäten basiert, dessen Netzwerke im Laufe der Evolution übernommen und weiterentwickelt wurden.