Use-dependent changes in synaptic strength play a fundamental role in shaping synaptic connections during development and provide a cellular basis for cognitive functions in the mature brain. Mounting epidemiological and genetic evidence highlight synaptic dysfunctions in the etiology and progression of a broad range of neurological disorders, and this underscores the central importance of synaptic processing. Each principal neuron in the brain receives many thousands of synaptic connections. Whereas synapses are functionally autonomous, nearby synapses strongly interact, and therefore, in deciphering how neural circuits exploit synaptic plasticity to encode and decode information, it is crucial to understand how synapses influence each other in adjusting their strengths. Using a combination of electrophysiology and imaging approaches we have investigated how synaptic strengths are dynamically distributed across the dendritic tree of hippocampal pyramidal neurons. We find that, surprisingly, postsynaptic strengths are homogeneous and cannot be discriminated between different inputs. In contrast, presynaptic strengths are distinct between convergent inputs targeting the same postsynaptic neuron, and inducing synaptic plasticity in one input triggers a compensatory change in the presynaptic strength of a non-stimulated input. We provide evidence for a novel cellular mechanism in balancing synaptic strengths across different synaptic connections.