Magnitude Codes for Cross-Modal Working Memory in the Primate Frontal Association Cortex

Abstract

Quantitative features of stimuli may be ordered along a magnitude continuum, or line. Magnitude refers to parameters of different types of stimulus properties. For instance, the frequency of a sound relates to sensory and continuous stimulus properties, whereas the number of items in a set is an abstract and discrete property. In addition, within a stimulus property, magnitudes need to be processed not only in one modality, but across multiple modalities. In the sensory domain, for example, magnitude applies to both to the frequency of auditory sounds and tactile vibrations. Similarly, both the number of visual items and acoustic events constitute numerical quantity, or numerosity. To support goal-directed behavior and executive functions across time, magnitudes need to be held in working memory, the ability to briefly retain and manipulate information in mind. How different types of magnitudes across multiple modalities are represented in working memory by single neurons has only recently been explored in primates. These studies show that neurons in the frontal lobe can encode the same magnitude type across sensory modalities. However, while multimodal sensory magnitude in relative comparison tasks is represented by monotonically increasing or decreasing response functions ("summation code"), multimodal numerical quantity in absolute matching tasks is encoded by neurons tuned to preferred numerosities ("labeled-line code"). These findings indicate that most likely there is not a single type of cross-modal working-memory code for magnitudes, but rather a flexible code that depends on the stimulus dimension as well as on the task requirements.

Keywords: frequency; monkey; neuronal coding; number; pre-SMA; prefrontal cortex; single neurons.

Figure 1

Cross-modal representation of flutter frequency in pre-SMA. (A) Delayed flutter discrimination task. The monkey is required to compare the frequency of two stimuli (first sample, then test) presented sequentially over a delay period between them. In the cross-modal condition, vibrotactile (top) or auditory flutter sample frequencies (bottom) are compared to auditory flutter or vibrotactile frequencies (respectively). (B) Time course of a PFC neuron responding monotonically to vibrotactile flutter frequencies during the sample and delay periods. Colors correspond to frequencies (Permission has been obtained from the copyright holder for the reproduction of this image from Romo and Salinas, 2003). (C) Monotonically increasing (neuron #1) and decreasing (neuron #2) response functions during the memory delay of two pre-SMA example neurons to both vibrotactile (blue) and auditory flutter frequencies (red). (from Vergara et al., 2016).

Figure 2

Cross-modal representation of numerosity in PFC. (A) Delayed match-to-numerosity task. In the sample phase, the monkey had to enumerate either visual items (top) or sound pulses (bottom), and memorize the numerosity in a delay period. After the delay, the monkey had to respond if the test dot array showed the same numerosity, and withhold response if it did not (probability 50%). In the visual trial condition, one to four dots were presented in the sample phase. In the auditory condition, one to four sound pulses were played. (B) Example PFC neuron (tested with visual numerosities 1 to 30) that was tuned to numerosity 6 both during sample presentation (gray) and memory delay (pink). Left: Spike density functions (only a selection of numbers shown for clarity). Colors correspond to specific tested numbers. Right: Tuning functions of this neuron during the sample (bottom) and delay period (top). (from Nieder, 2016) (C) Average normalized numerosity tuning functions of supramodal PFC neurons in the delay period. (from Nieder, 2012).