On-line, voluntary control of human temporal lobe neurons

Abstract

The brain has to continually select between a plethora of external sensory stimuli in order to focus on and process a few of them. Neurons in the medial temporal lobe (MTL) are selectively responsive to particular visual objects, and their activity is known to be modulated by cognitive effects. Cerf et al. have constructed a new brain–machine interface in which patients implanted with intracranial electrodes looking at superimposed computer images, when asked to make an image fade in or fade out, rapidly learnt to regulate neuronal activity of their MTL neurons in different subregions and hemispheres. They were able to increase the firing rate of certain cells while decreasing that of others and controlling the composite image content. This work provides direct evidence that humans can control the neuronal activity of their own visual neurons deep inside their own brain, and that such activity can be decoded to control devices. It is hoped that similar interface devices will one day boost the communication of patients with various neurological impairments, such as locked-in syndrome or motor neuron disease. Neurons in the medial temporal lobe are selectively responsive to particular visual objects, but their activity is modulated by internal cognitive effects. Here it is shown that humans can regulate the activity of their MTL neurons to alter the outcome of the contest between external images and their internal representation. Using a brain–machine interface, subjects looked at a hybrid superposition of two images and had to enhance one image at the expense of the other, using cognitive strategies such as attention and imagery. Daily life continually confronts us with an exuberance of external, sensory stimuli competing with a rich stream of internal deliberations, plans and ruminations. The brain must select one or more of these for further processing. How this competition is resolved across multiple sensory and cognitive regions is not known; nor is it clear how internal thoughts and attention regulate this competition1,2,3,4. Recording from single neurons in patients implanted with intracranial electrodes for clinical reasons5,6,7,8,9, here we demonstrate that humans can regulate the activity of their neurons in the medial temporal lobe (MTL) to alter the outcome of the contest between external images and their internal representation. Subjects looked at a hybrid superposition of two images representing familiar individuals, landmarks, objects or animals and had to enhance one image at the expense of the other, competing one. Simultaneously, the spiking activity of their MTL neurons in different subregions and hemispheres was decoded in real time to control the content of the hybrid. Subjects reliably regulated, often on the first trial, the firing rate of their neurons, increasing the rate of some while simultaneously decreasing the rate of others. They did so by focusing onto one image, which gradually became clearer on the computer screen in front of their eyes, and thereby overriding sensory input. On the basis of the firing of these MTL neurons, the dynamics of the competition between visual images in the subject’s mind was visualized on an external display.